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Gram-type Positive Advanced article

Bacteria . Introduction
Article Contents

Juergen Wiegel, University of Georgia, Athens, Georgia, USA . Phenotypic Definition and Phylogenetic Coherence

. Evolution within the Domain Bacteria


Dorothy E Byrer, University of Georgia, Athens, Georgia, USA . Phylogeny and Taxonomy
Rob Onyenwoke, Kenyon College, Gambier, Ohio, USA . The Phylum Firmicutes (Classes Clostridia, Mollicutes and
Bacilli)
Based in part on the previous version of this Encyclopedia of Life Sciences . Major Firmicutes Properties: Cell Wall Structure and
(ELS) article, Gram-type Positive Bacteria by Dorothy E Byrer and Endospore Formation
Juergen Wiegel.
. Physiological Properties of Firmicutes

. Class Mollicutes: Mycoplasmas and Relatives


Gram-type positive bacteria, composed of the two phyla Firmicutes and Actinobacteria,
. The Phylum Actinobacteria (Class Actinobacteria)
are characterized by the presence of a thick peptidoglycan layer and the absence of
. Physiological Diversity
lipopolysaccharide and an outer membrane. Though closely related phylogenetically,
. Medical Aspects
these bacteria are diverse in habitat, metabolism and medical and industrial
. Spoiling Organisms
importance. Although not observed for all, the Firmicutes (low G + C mol% group)
. Habitats and Ecology
represent endospore-formers while the Actinobacteria (high G + C mol% group) taxa
. Biotechnological Aspects of Firmicutes and Actinobacteria
form actinospores (Actinoplanes), conidiospores (Streptomyces) or hyphae-
. Conclusion
fragmentation into short cells without formation of conidia (Nocardia).
doi: 10.1002/9780470015902.a0000456.pub2

Introduction Antibiotic Resistance; Bacterial Capsules and Evasion of


Immune Responses; Bacterial Cells; Classification;
Antonie van Leeuwenhoek devised the first grouping of Leeuwenhoek, Antoni van; Phylogenetics
bacteria in the seventeenth century when he described ba- This entry discusses the phenotypic and phylogenetic
cilli, cocci and spirals (reviewed in Bozzola and Russell, determinants and the evolutionary relatedness of the
1992). In 1884, Christian Gram discovered that the differ- Gram-type positive bacteria based on 16S ribosomal ribo-
ential uptake and retention of a crystal violet–iodide stain nucleic acid (16S rRNA) sequence data used today for sys-
combination by bacterial cells, when treated with organic tematic and phylogenetic classification of bacteria (Woese
solvents (ethanol or isopropanol) and counterstained with et al., 1990). Attention will be given to both organisms
saffranin, divided them into two distinct groups. The first traditionally classified as ‘Gram (staining) positive’, as well
group encompassed cells which incorporated the primary as to those which phylogenetically belong to this group of
stain, retained it, and thus appeared dark blue or purple – ‘Gram-type’ positives (Wiegel, 1981) based on molecular
termed Gram (staining) positive. The second group of cells classification methods, especially 16S rRNA sequence
did not retain the primary stain but took up the counter- analyses. Taxonomic and systematic classification is in
stain, thus appearing pink – termed Gram (staining) neg- flux and, with more and more novel taxa described every
ative (Gram, 1884). Subsequently, important physiological month, will be constantly modified and rectified. The im-
and structural differences, e.g. virulence patterns and an- portance of these bacteria in medicine, industry, food and
tibiotic sensitivities, were observed which correlated with scientific research will be discussed, and a comparison of
the differential staining characteristics. Despite the exist- the various habitats and ecological niches of this diverse
ence of bacteria that do not stain consistently, or at all, the group will be presented. For detailed information on the
Gram staining reaction has remained an important taxo- various taxa or physiological groups, the reader is referred
nomic property in the day-to-day identification of bacteria, to the new multivolume editions of the Bergey’s Manual of
especially clinical isolates. To differentiate between the Systematic Bacteriology and to The Prokaryotes. See also:
phylogenetic position and the taxonomic staining property Classification; Molecular Genetics; rRNA Genes: Evolu-
Wiegel (1981), Wiegel and Quandt (1982) introduced the tion; rRNA Structure
term ‘Gram-type’ to describe the phylogenetic position and
proposed that the term ‘Gram staining’ or ‘Gram reaction’
be used for describing the result of staining (see later for
further explanation). For clarity and to avoid misunder- Phenotypic Definition and
standings, the short terms ‘Gram positive’ and ‘Gram Phylogenetic Coherence
negative’ should be avoided or at least not used without
clarification whether one is referring to the phylogenetic The typical Gram-type negative bacterium has its cyto-
position or to the staining reaction. See also: Bacterial plasm bounded by a lipid bilayer (the cytoplasmic

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 1
Gram-type Positive Bacteria

membrane), which is surrounded by a thin layer of the alternating N-acetylmuramic acid and N-acetylglucosa-
peptidoglycan murein (Figure 1a). Around this is another mine with various side-chains, which may be crosslinked
lipid bilayer, which is biochemically and physiologically either directly or via polypeptide chains containing a va-
distinct from the first and which is termed the outer mem- riety of amino acids. These variations have been used to
brane. The presence of these two membranes creates the create the taxonomically important cell wall types
periplasmic space between them, important in the physi- (Schleifer and Kandler, 1972). The Gram-type negative
ology of the Gram-type negative cell as well as in its dis- cell walls usually have direct crosslinking of the muramic
tinction from the Gram-type positive cell which – based on acid chains (the meso-diaminopimelic acid direct type=
the generally accepted notion – lacks the periplasmic space. m-DAP type), while the ‘typical’ Gram-type positive cell
However, the argument persists as to whether a pseudo- walls contain polypeptide chains as crosslinkers. However,
periplasmic space exists in the Gram-type positive bacteria many clostridial species (Clostridium sensu stricto, order
(Merchante et al., 1995). Attached to the outer leaf of the Clostridiales; Rainey et al., 2006; Wiegel, 2007) and mem-
outer membrane in the Gram-type negative cell is a layer of bers of the Thermoanaerobacteriaceae order Therm-
lipopolysaccharide (LPS), which (1) is important antigen- anaeroobacteriales (Onyenwoke and Wiegel, 2008) and
ically, (2) has significance in pathogenesis and virulence related genera/species also have the m-DAP type. But, in
and (3) is not found in Gram-type positive bacteria. In comparison to Gram-type negative cells, these clostridial
contrast, the typical Gram-type positive bacterium has an species have a higher content of muramic acid or
envelope which consists of a cell membrane surrounded by N-acetylmuramic acid and N-acetylglucosamine,=thicker
a thick layer of murein, which often contains teichoic or wall (see later under Taxonomy for the different cell wall
teichuronic acid side-chains (Figure 1b). Murein consists of types). The basis for the Gram staining reaction is the thick
layers of polypeptide chains which are crosslinked by mu-
rein in Gram-type positives do not readily allow organic
LPS solvents to penetrate and remove the crystal violet–iodide
stain, whereas the thin layer of directly crosslinked murein in
the Gram-type negatives does. In fact, the primary stain may
OM
actually damage the Gram-type negative cell wall, allowing
loss of the stain upon solvent treatment and subsequent
uptake of the counterstain (Popescu and Doyle, 1996).
See also: Bacterial Cell Wall; Bacterial Cytoplasmic Mem-
M P brane; Lipopolysaccharides
The differentiation by Gram staining reaction generally
works well with most clinical isolates (for an exception, see
O’Brien and George, 1997), but is frequently equivocal
with soil and sediment bacteria, especially thermophiles
CM
because their murein sacculus can be thinner or less exten-
sively crosslinked. Generally Gram-type negative cells
contain about 10% murein, whereas Gram-type positives
(a) C contain around 20% murein. However, there are excep-
tions on both sides, e.g. species of the Gram-type negative
Alphaproteobactera Xanthobacter contain about 15% mu-
rein but when grown under certain conditions substitute
the cell wall with a glutamine polymer, leading to a far
lower 10% murein content, and the presence of many in-
M tracellular polyphosphate granula can lead to the false in-
terpretation of a Gram positive staining. Some Gram-type
positive bacteria, e.g. some species of Clostridium, Bacillus
and Thermoanaerobacteriaceae, stain Gram negative at all
stages of growth but, based on their cell envelope and mo-
lecular systematic features, clearly belong to the Gram-
CM type positive branch (Wiegel, 1981). Similar examples are
the so-called Gram stain-variable bacteria, such as Art-
hrobacter species from the Actinobacteria phylum, which
only stain Gram positive in the very early exponential
(b) C
growth phase. After further growth, their cell wall becomes
Figure 1 Envelope structure of (a) the ‘typical’ Gram-type negative thinner and the Gram staining reaction is negative. Two
bacterium; and (b) the ‘typical’ Gram-type positive bacterium. LPS, other important examples where the Gram staining reac-
lipopolysaccharide; OM, outer membrane; P, periplasm; M, murein; tion and the Gram-type do not coincide are the medically
CM, cytoplasmic membrane; C, cytosol. important mycoplasma and mycobacteria. The first group

2 ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net
Gram-type Positive Bacteria

has no cell wall, and the second has an outer layer con- R.H. Vreeland, personal communication) Thus, Murray’s
taining waxes which do not allow uptake of the crystal classification has become outdated, but the term ‘Firmi-
violet–iodide stain. For both of these, the Gram stain is cutes’ is retained. In the current (generally accepted) 16S
meaningless. Although the Gram staining reaction can be rRNA sequence analysis-based phylogenetic tree (Figure 2),
used to differentiate archaea taxonomically into Gram all bacteria previously classified as Gram-type positive be-
staining positive and negative groups, they do not fit into long to one major bifurcated branch containing the phyla
Gram’s original classification for bacteria because these Firmicutes and Actinobacteria. However, the 16S rRNA
organisms contain only a pseudomurein sacculus or exclu- sequence analysis also currently includes a few genera in
sively a proteineous cell wall lacking LPS (Beveridge and this branch which, based on their cell wall structure and
Schultze-Lam, 1996). Consequently, archaea that stain presence of LPS, (e.g. Sporomusa and Megasphaera)
Gram reaction positive are usually not included when the ‘should’ belong to one of the groups of the Gram-type
imprecise short term ‘Gram positive microorganism’ is negative bacteria. See also: Darwin, Charles Robert;
used, as this term sensu stricto refers only to bacteria. Evolutionary Ideas: Darwin; Phylogeny Based on 16S
See also: Archaeal Cell Walls rRNA/DNA; Polymerase Chain Reaction (PCR); Pro-
Thus, a clear differentiation of Gram-terms avoids the karyotic Systematics: a Theoretical Overview
confusion of having ‘Gram negative’ species in a ‘Gram
positive’ genus or family, and the above-noted terminology
(Gram-type versus Gram reaction/staining) is used Evolution within the Domain Bacteria
throughout this article. To discriminate between Gram
staining negative but Gram-type positive bacteria and Presently, the general phylogenetic tree divides life into
Gram-type negative bacteria, the formation of the poly- three domains: the Bacteria, the Eukarya and the Archaea
myxin B-LPS complex structures, i.e. braided structures of (Woese et al., 1990). Among the domain Bacteria, members
LPS-polymyxin in solution or as blebs on polymyxin B – of the order Thermatogales appears to be the oldest, i.e.
treated cells observed in electron micrographs, is used most deeply branching group of the bacteria. (For an over-
(Wiegel and Quandt, 1982). This method is based on the view of origin of life and evolution see chapters in Wiegel
assumption only Gram-type negative bacteria possess LPS. and Adams, 1998) Many authors place the green nonsulfur
However, very recently it appears that some Gram-type bacteria on the next ‘branch’, with the radiation-resistant
positive Firmicutes, e.g. Megasphaera of family Acid- micrococci (Deinococcus and related) arising next. The
aminococcaceae (based on the taxonomic outline for Gram-type positives, the purple bacteria and cyanobacte-
the new edition of Bergey’s Manual for Systematic ria may form the next evolving groups (Woese et al., 1990).
Bacteriology http://141.150.157.80/bergeysoutline/outline/ The cyanobacteria and purple bacteria are Gram-type
bergeysoutline_5_2004.pdf) within the order Clostridiales negative microorganisms that are closely related to the
of the class Clostridia, possess LPS. In the future, it may Gram-type positives, and the cyanobacteria may well be
become prudent for a precise terminology to totally aban- the progenitor of the other two groups. The anoxygenic
don the use of Gram-classification and to only use the photosynthetic purple bacteria seem more closely related
staining reaction as a simple property to taxonomically – to the oxygenic photosynthetic cyanobacteria and to the
but not phylogenetically-characterize an isolate and oth- nonphotosynthetic Gram-type positives than to the anox-
erwise use the phyla terms of Firmicutes and Actinobacteria ygenic green photosynthetic bacteria. The mycoplasma
(see later). group, unable to synthesize peptidoglycan precursors and
Since the 1859 publication of Darwin’s On the Origin of thus lacking cell walls and being resistant to the antibiotics
Species, classification of bacteria and other organisms has which act by disrupting cell wall components, seems to
aimed at correctly delineating actual genetic and evolu- have evolved from the low G+C clostridial branch of the
tionary relatedness – phylogeny. Based on cell envelope Gram-type positive bacteria. See also: Bacterial Evolution;
structure, Murray suggested grouping bacteria into four Bacterial Origins; Cyanobacteria; Green Sulfur Bacteria;
divisions: ‘Firmicutes’, which are Gram-type positive; Photosynthesis; Photosynthesis and Respiration in
‘Gracilicutes’, which are Gram-type negative; ‘Teneri- Cyanobacteria
cutes’, which have no cell wall and ‘Mendosicutes’, which
are the archaea (Murray, 1984). Presently the use of 16S
rRNA – isolated from the 30S ribosomal subunits – (16S Phylogeny and Taxonomy
rRNA) sequence comparison analysis is thought to be the
best approach for a phylogenetic classification. These se- Because the taxonomy, phylogeny and nomenclature within
quences are highly conserved, change very slowly from an the Gram-type positive bacteria is currently in a state of flux,
evolutionary standpoint and are felt to represent true relat- the reader is referred to the new editon of Bergey’s Manual of
edness among bacteria. However, it should be mentioned Systematic Bacteriology – now appearing as a new multi-
that some recent analysis has called into question the va- volume edition (http://141.150.157.80/bergeysoutline/
lidity of using the 16S rRNA sequences as a type of phylo- outline/bergeysoutline_5_2 004.pdf.) and the searchable
genetic clock, as this is a practice which includes some website from J.P. Euzéby: List of Prokaryotic Names with
unproven assumptions (Vreeland and Rosenzweig, 2002; Standing in Nomenclature (http://www.bacterio.cict.fr/

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 3
4
T
*Streptococcus pyogenes DSM 20565 (AB002521) Streptococcaceae
T
*Lactobacillus delbrueckii subsp. delbrueckii DSM 20074 (M58814) Lactobacillaceae
T
*Leuconostoc mesenteroides subsp. mesenteroides DSM 20343 (M23035) 'Leuconostocaceae' Order II
'Lactobacillales'
T
*Carnobacterium divergens DSM 20623 (M58816) 'Carnobacteriaceae'
810
T
*Enterococcus faecalis DSM 20478 (AB012212) 'Enterococcaceae'
T
*Aerococcus viridans DSM 20340 (M58797) 'Aerococcaceae'

T
930 *Planococcus citreus DSM 20549 (X62172) Planococcaceae
T
Gram-type Positive Bacteria

Class III *Caryophanon latum NCIB 9533 (X70314) Caryophanaceae


‘Bacilli’
T
*Listeria monocytogenes DSM 20600 (X56153) 'Listeriaceae'

T
Sporolactobacillusinulinus DSM 20348 (M58838) 'Sporolactobacillaceae'
T Order I
Bacillussubtilis subsp. subtilis DSM 10 (AJ276351) Bacillaceae
Bacillales
T
*Staphylococcus aureus subsp. aureus DSM 20231 (D83357) 'Staphylococcaceae'
T
*Turicibacter sanguinis DSM 14220 (AF349724) 'Turicibacteraceae'
T
Thermoactinomyces vulgaris DSM 43016 (M77491) 'Thermoactinomycetaceae'

T
Paenibacilluspolymyxa DSM 36 (D16276) 'Paenibacillaceae'
T
Alicyclobacillus acidocaldarius subsp. acidocaldarius DSM 446 (X60742) 'Alicyclobacillaceae'

T
*Erysipelothrix rhusiopathiae DSM 5055 (M23728) 'Erysipelotrichaceae' Order V Incertae sedis
T
*Anaeroplasma abactoclasticum ATCC 27879 (M25050) Anaeroplasmataceae Order IV Anaeroplasmatales
1000
Class II 850 T
Mollicutes *Acholeplasma laidlawii ATCC 23206 (U14905) Acholeplasmataceae Order III Acholeplasmatales
T
*Entomoplasma ellychniae ATCC 43707 (M24292) Entomoplasmataceae
790 1000
Order II Entoplasmatales
T
1000 *Spiroplasma citri ATCC 27556 (M23942) Spiroplasmataceae
Order I Myco-
T plasmatales
*Mycoplasma pneumoniae ATCC 15531 (M29061) Mycoplasmataceae

T
1000 *Halobacteroides halobius DSM 5150 (U32595) Halobacteroidaceae Order III
Haloanaerobiales
T
*Halanaerobium praevalens DSM 2228 (M59123) Haloanaerobiaceae
T
*Eubacterium limnosum DSM 20543 (M59120) 'Eubacteriaceae' Order I Clostridales
T Order II
1000 Thermoanaerobacterium thermosulfurigenes DSM 2229 (L09171) 'Thermoanaerobacteriaceae' 'Thermo-
T
*Syntrophomonas wolfei subsp. wolfei DSM 2245 (AF022248) Syntrophomonadaceae anaerobacteriales'
T
*Peptococcus niger DSM 20475 (X55797) Peptococcaceae

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net
Class I T
'Clostridia' *Heliobacterium chlorum ATCC 35205 (M11212) 'Heliobacteriaceae'
Order I
T Clostridales
*Acidaminococcus fermentans DSM 20731 (X65935) 'Acidaminococcaceae'
T
Lachnospira pectinoschiza ATCC 49827 (L14675) 'Lachnospiraceae'

T
710 *Peptostreptococcus anaerobius ATCC 27337 (D14150) 'Peptostreptococcaceae'
T
Clostridium butyricum DSM 552 (M59085) Clostridiaceae
T
*Escherichia coli DSM 30083 (X80725)

(a) 0.05
Gram-type Positive Bacteria

search.html). Start your search with the terms Firmicutes and they (1) have more typical Gram-type negative cell enve-
Actinobacteria (phyla). lopes, (2) do not sporulate and (3) apparently lack the ma-
The ‘Gram-type positive bacteria’ all belong to one of the jor sporulation-specific genes (Onyenwoke et al., 2004).
two bacterial phyla, i.e. Phylum BXIII Firmicutes (previ- Using genomic DNA sequence analysis, Onyenwoke et al.
ously also called the low G+C group= 560 mol% G+C) (2004 and literature cited therein) again demonstrated that
and Phylum BXIV Actinobacteria (the high G+C the property of forming endospores does not always cor-
group= 460 mol% G+C) (Figure 2a and b). The myriad relate well with 16S rRNA trees. In general, the endo-
of traditional taxonomic schemes such as numerical tax- sporulating rods, the regular nonsporulating rods and the
onomy, the Gram staining reaction, cellular and colonial cocci have a low G+C content, while the irregular-shaped,
morphology, metabolic capabilities such as substrate uti- frequently branching or at least polymorphic nonsporu-
lization profiles or fermentation product ratios, biochem- lating rods have a high G+C content and are grouped with
ical composition, structural characteristics such as cell wall the actinomycetes and mycobacteria. Exceptions are the
analysis, and growth parameters such as temperature and genera Thermobrachium and Anaerobranca, which belong
pH were all used to group organisms into the different to the Firmicutes despite their branching morphology
genera. But today they are used mainly for taxonomic (Engle et al., 1996). See also: Bacterial Endospores; Bac-
differentiation/characterization of species but not for basic terial Fermentation; Clostridia; Bacillus subtilis as a Model
phylogenetic classification. The 16S rRNA sequence anal- for Bacterial Systems Biology
ysis has confirmed, more or less, the major divisions based In the distant past, all aerobic and facultatively anaer-
on the deoxyribonucleic acid (DNA) G+C content into obic sporulating rods were classified within the genus Ba-
the low (Firmicutes) and high (Actinobacteria) G+C con- cillus, and all obligately anaerobic rods were classified
tent phyla. Within each of these groups, an important tax- within the genus Clostridium. An exception was the
onomic characteristic was the presence or absence of the obligately anaerobic sporulating sulfate reducers, which
ability to form spores, the endospores of the Firmicutes were placed in a separate genus, Desulfotomaculum. This
and the actino- or conidiospores of the Actinobacteria. led to genera with a G+C mol% ranging from 22 to 56,
However, since about 75 gene products are sequentially illustrating that the genera were ill-defined. Attempts to
required for endospore formation in Bacillus subtilis, reclassify and divide these genera failed until 16S rRNA
the absence of spore formation is no longer regarded sequence analysis became available. Based on this, the
as a strong phylogenetic property. True endospores are – genera are now in the process of being broken up into more
so far – only formed by the Firmicutes. However, while no defined groups and novel genera, leaving those species very
Gram-type negative bacterium has been described to closely related to B. subtilis and Clostridium butyricum (the
form endospores, not all class Clostridia and Bacilli type species of the type genera of the type families Ba-
bacteria form endospores (Brill & Wiegel, 1997; cillaceae and Clostridiaceae of the orders Bacillales and
Onyenwoke et al., 2004) (see later for more discussion on Clostridiales, respectively) classified as true Bacillus and
spore formation). Sporomusa represents a special case: Clostridium species, i.e. species sensu stricto.
it is a genus with sporulating cells, but a Gram-type The so-called ‘Bacillus’ subbranch (order Bacillales)
negative envelope structure. Its 16S rRNA sequence places presently includes, beside the true Bacillus species, genera
members of this genus, along with Megasphaera, Se- such as Brevibacillus, Aneurinibacillus and Paenibacillus, as
lenomonas, Butyrivibrio, Pectatus and Zymophilus, among well as those aerobic sporulating rods still (ill-)classified as
the Gram-type positive endospore-formers even though Bacillus species.

Figure 2 (a) Phylogenetic tree for the families of the phylum Firmicutes. This neighbour-joining tree shows the estimated phylogenetic relationships for the type
strains of the type species of the type genera for each family contained within the phylum ‘Firmicutes’ based on 16S rRNA gene sequence data with Jukes–Cantor
correction for synonymous changes. The 16S rRNA gene data used represent Escherichia coli DSM 30083T nucleotide positions 78–1514. Numbers at nodes
indicate bootstrap support values for 1000 replicates. Bar indicates 0.05 nucleotide substitutions per site. The symbol ‘’ before the strain name indicates the
strain has never been shown to produce endospores. The superscript ‘T’ denotes the sequence is from the type strain for the type species of the type genus for the
corresponding family within the phylum ‘Firmicutes’. GenBank accession numbers are given in parentheses. Family names are indicated in bold after the GenBank
accession number. The three classes of the ‘Firmicutes’ are indicated by dashed lines. Lachnospira multipara and Mycoplasma mycoides subsp. mycoides are the type
species for the genera Lachnospira and Mycoplasma, respectively, however, full length 16S rRNA data are not available for either species. Therefore, Lachnospira
pectinoschiza and Mycoplasma pneumoniae were included to represent those genera. In addition, endospore-formation has never been demonstrated for
L. multipara but has been demonstrated for L. pectinoschiza. No 16S rRNA sequence is available for the nonendospore-forming Acetoanaerobium noterae, a
member of the Class III ‘Bacilli’ Order II ‘Lactobacillales’. (b) Phylogenetic tree of families of the phylum Actinobacteria. Neighbour-joining tree shows the
estimated phylogenetic relationships for the type strains of the type species of the type genera for each family contained within the phylum Actinobacteria based
on 16S rRNA gene sequence data with Jukes–Cantor correction for synonymous changes. The 16S rRNA gene data used represent E. coli DSM 30083T nucleotide
positions 161–1361. Numbers at nodes indicate bootstrap support values for 1000 replicates. Bar indicates 0.05 nucleotide substitutions per site. Many taxa
produce actino- or conidiospores, however, species indicated by ‘’ have never been observed to produce any spores. The superscript ‘T’ denotes the sequence is
from the type strain for the type species of the type genus for the corresponding family within the Phylum Actinobacteria. GenBank accession numbers are given in
parentheses. Family name is indicated in bold after the GenBank accession number. The five subclasses of the Actinobacteria are indicated as well as the two orders
contained within Subclass V Actinobacteridae. Two sporulating strains from Subclass V Actinobacteridae, Kineosporia aurantiaca (Order I Actinomycetales) and
Actinobispora yunnanensis (Order II Bifidobacteriales), were omitted from the tree due to their current, unclear taxonomic statuses. No 16S rRNA sequence is
available for the spore-forming Frankia alni, a member of the Subclass V Actinobacteridae, Order I Actinomycetales.

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 5
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Gram-type Positive Bacteria


T
*Actinomyces bovis DSM 43014 (X53224) Actinomycetaceae
T
*Beutenbergia cavernae DSM 12333 (Y18378) 'Beutenbergiaceae'
T
*Bogoriella caseilytica DSM 11294 (Y09911) Bogoriellaceae
T
Promicromonospora citrea DSM 43110 (X83808) Promicromonosporaceae
T
*Brevibacterium linens DSM 20425 (X77451) Brevibacteriaceae
T
760 *Jonesia denitrificans DSM 20603 (X78420) Jonesiaceae
T
*Dermabacter hominis DSM 7083 (X91034) Dermabacteraceae
T
*Micrococcus luteus DSM 20030 (AJ536198) Micrococcaceae
T
950 Intrasporangium calvum DSM 43043 (D85486) Intrasporangiaceae
750 T
ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net

*Dermacoccus nishinomiyaensis DSM 20448 (X87757) Dermacoccaceae


T
Dermatophilus congolensis DSM 44180 (M59057) Dermatophilaceae
T
*Microbacterium lacticum DSM 20427 (X77441) Microbacteriaceae
T
*Sanguibacter keddieii DSM 10542 (X79450) Sanguibacteraceae
T
*Cellulomonas flavigena DSM 20109 (X83799) Cellulomonadaceae
T
*Rarobacter faecitabidus DSM 4813 (Y17870) Rarobacteraceae
T
920 *Dietzia maris DSM 43672 (X81920) Dietziaceae
T
*Tsukamurella paurometabola DSM 20162 (X53206) Tsukamurellaceae
T
Order I Actinomycetales *Corynebacterium diphtheriae DSM 44123 (X82059) Corynebacteriaceae
T
*Nocardia asteroides DSM 43373 (X84850) Nocardiaceae
*Williamsia muralis DSM 44343T(Y17384) 'Williamsiaceae'
T
*Mycobacterium tuberculosis subsp. tuberculosis ATCC 27294 (X55588) Mycobacteriaceae
Subclass V T
*Gordonia bronchialis DSM 43247 (X79287) Gordoniaceae
Actinobacteridae T
Actinosynnema mirum DSM 43827 (X84447) Actinosynnemataceae
T
Pseudonocardia thermophila DSM 43832 (X53195) Pseudonocardiaceae
T
*Nocardioides albus DSM 43109 (X53211) Nocardioidaceae
T
*Propionibacterium freudenreichii subsp. freudenreichii DSM 20271 (X53217) Propionibacteriaceae
T
Streptomyces albus subsp. albus DSM 40313 (AJ621602) Streptomycetaceae
T
Micromonospora chalcea DSM 43026 (U58531) Micromonosporaceae
T
*Microsphaera multipartita DSM 44233 (Y08541) Microsphaeraceae
T
Sporichthya polymorpha DSM 43042 (AB025317) Sporichthyaceae
T
Geodermatophilus obscurus DSM 43160 (X92356) Geodermatophilaceae
T
*Acidothermus cellulolyticus DSM 8971 (AJ007290) Acidothermaceae
T
Streptosporangium roseum DSM 43021 (X89947) Streptosporangiaceae
T
Thermomonospora curvata DSM 43183 (X97893) Thermomonosporaceae
T
Nocardiopsis dassonvillei subsp. dassonvillei DSM 43111 (X97886) Nocardiopsaceae
T
Glycomyces harbinensis DSM 46494 (D85483) Glycomycetaceae
T
*Bifidobacterium bifidum DSM 20456 (M38018) Bifidobacteriaceae Order II Bifidobacteriales
*Coriobacterium glomerans DSM 20642T(X79048) Coriobacteriaceae Subclass III Coriobacteridae
T
* Acidimicrobium ferrooxidans DSM 10331 (U75647) Acidimicrobiaceae Subclass I Acidimicrobidae
T
*Sphaerobacter thermophilus DSM 20745 (AJ420142) Sphaerobacteraceae Subclass IV
T
*Rubrobacter radiotolerans DSM 46359 (X87134) Rubrobacteraceae Subclass II Rubrobacteridae Sphaerobacteridae
T
*Escherichia coli DSM 30083 (X80725)

(b) 0.05

Figure 2 (Continued)
Gram-type Positive Bacteria

The class Clostridia taxa, so-called ‘Clostridium’ Order I Bacillales with 10 families containing many
subbranch, contains, beside the true Clostridium species novel genera created from the ‘old’=pre-16S rRNA se-
in the order Clostridiales, a great variety of well- and less quence taxonomy and ill-defined genus Bacillus and
well-known genera of Gram-type positive rods and cocci, Order II Lactobacillales with six families and an un-
e.g. Lactococcus, Staphylococcus, Streptococcus, Sporolacto- placed taxa, the group ‘Incertae sedis’.
bacillus, and the Gram-type negative Sporomusa and
The two classes Clostridia and Bacilli contain species
Megasphaera. The order Thermoanaerobacteriales so far in-
with a great variety of physiological types (see later).
cludes genera consisting only of anaerobic thermophiles, e.g.
genera such as Anaerobranca, Thermoanaerobacterium,
Thermoanaerobacter, Moorella and Caloramator. The third
and fourth order Halanaerobiales and Natranaerobiales, re-
Major Firmicutes Properties: Cell Wall
spectively, contain only anaerobic halophiles. Structure and Endospore Formation
The old division into (facultative) aerobic and obligately
anaerobic subbranches has also become obsolete, e.g. the For the Firmicutes, an important distinguishing property is
obligately anaerobic, iron(III) reducer Bacillus infernus, the cell wall structure – leading to the peptidoglycan
clusters, as the name correctly indicates, within the ‘Bacil- classes. Regarded as a phylogenetic property, peptidogly-
lus’ subbranch (Boone et al., 1995), whereas the aerobic can classes are determined based on (1) mode of glycan
Thermaerobacter marianensis clusters with the obligately crosslinking (groups A and B), (2) presence and type of
anaerobic Moorella and Thermoanaerobacter spp. (Takai interpeptide bridge (subgroups 1–5), (3) amino acid
et al., 1999). present in position 3 of the stem peptide (variations a to
Currently, the large genera Clostridium and Bacillus are d) and (4) amino acid sequence of the peptide moiety (types)
undergoing further major taxonomic rearrangements (Schleifer and Kandler, 1972; Scott and Barnett, 2006).
based on 16S rRNA sequence analyses, leading to many Peptidoglycan classes usually correlate well with other
novel genera (see for example Collins et al., 1994). In the phylogenetic groupings, e.g. the mycobacteria have vari-
case of medically important organisms, recognition may ants of class A-2, spirochaetes contain A-1-b, the non-
prove more important than phylogenetic accuracy, and sporulating Gram-type positive bacteria have A-3 or A-4
historic names may well be retained in some cases, although and some coryneform bacteria and anaerobic act-
most of the medically important species belong to the inomycetes contain a class B-1 or B-2 cell wall type. Var-
Clostridum sensu stricto clade. iation in the content of lipids, glycoproteins and other
antigenic markers, as well as susceptibility to phage is also
used to differentiate species and strains. Phage typing has
become especially important for the taxonomy of the
The Phylum Firmicutes (Classes high G+C content actinomycetes (Williams et al., 1993)
Clostridia, Mollicutes and Bacilli) and lactic acid bacteria. See also: Bacteriophages;
Peptidoglycan
The phylum Firmicutes is also informally called the Many members of the Firmicutes, – with the princi-
‘low G+C’ or ‘Bacillus–Clostridium’ branch. How- pal exception being the class Mollicutes – are exclusively
ever the latter term is misleading, since more and more able to form endospores as resting cells (as discussed
genera are found within this group which are not closely earlier). Generally cells produce one endospore per cell,
related to the former ‘catch them all’ genera Clostridium however, exceptions exist in the Clostridiales, a few
and Bacillus. Clostridium species produce two or more, e.g. Clostridium
Phylum BXIII Firmicutes presently contains three polysporum and Anaerobacter polyendosporus (Siunov
classes (Based on the Bergey’s Manual of Systematic Bac- et al., 1999). A very special case of spore formation as a
teriology outline, as of August 2007): means of multiplication occurs in Epulopiscium and
Class I Clostridia Metabacterium species which release ‘live bacteria cells’
using a process – at least – very similar to sporulation
(Angert et al., 1996). Endospores (in contrast to conidio-
Order I Clostridiales with more than 8 families,
and actinospores) are formed in a highly complex process
Order II Thermoanaerobacteriales with two families
involving asymmetrical cell division and the subsequent
containing – so far – only thermophiles,
engulfment of the smaller cell,=spore protoplast, by the
Order III Halanaerobiales with two families containing
‘mother cell’. The dry- and heat-resistant spore coat con-
only halophiles and
tains large amounts of Ca and spore-specific dipicolinic
Order IV Natranaerobiales containing halo-alkaliphilic
acid. The spore morphology varies and is usually species
taxa (Mesbah et al., 2007).
specific. Spores are either oval or spherical and are either
slightly smaller in diameter than the mother cell, causing no
Class II Mollicutes (with only one order, the Mycoplas- swelling of the mother cells, or significantly larger, leading
matales, and one family, the Mycoplasmataceae) and to a characteristic swelling of the mother cell (lemon-
Class III Bacilli with two orders shaped sporangium=a cell containing an endospore or

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 7
Gram-type Positive Bacteria

drumstick sporangium). An example is the thermophile the so-called ‘clostridial fermentation’ forming ethanol,
Clostridium thermocellum, which converts to long and acetate, lactate, butyrate, hydrogen and carbon dioxide in
thinner cells with cell-swelling terminal spores when enter- varying ratios. Most group 1 clostridia form at least some
ing the sporulation phase. The term ‘clostridial’ butyrate as one of their major products. More specialized
spores=‘drumstick-type’ and ‘bacillus’ spores=central pathways include the Strickland reaction, entailing oxida-
non-cell-swelling are outdated. There is only a slight pref- tion of one amino acid and reduction of another amino acid
erence among the anaerobes to form the drumstick-type of to yield its products, and the fermentation of ethanol by
sporangium. See also: Anaerobes Clostridium kluyveri to form butyrate or caproate. Many
clostridia-like taxa produce various volatile fatty acids in
trace amounts, frequently from the metabolism of amino
Physiological Properties of Firmicutes acids. (Gottschalk (1986) is an excellent resource.) See also:
Bacterial Fermentation; Glycolytic Pathway
Physiological properties of Firmicutes range from predom- Anaerobic respiration is based upon the use of various
inantly chemolithoautotrophs to glycolytic (cellulose-, compounds other than oxygen as electron acceptors via the
starch-, etc., utilizers) and peptidolytic bacteria. Some electron transport chain. In anaerobic Gram-type positive
have complex nutritional requirements, e.g. many of the bacteria, this includes using thiosulfate as electron acceptor
lactic acid bacteria. Also included are denitrifiers, aerobic while sulfide is formed as reduced compound (mechanism
and anaerobic nitrogen fixers, reductive dehalogenators, for forming elemental sulfur with no sulfide formation un-
anaerobic iron(III) reducers and a variety of aerobic and der strict anaerobic conditions is not clear and presently
anaerobic extremophiles, including moderate and extreme under investigation but occurs in cultures of Therm-
thermophiles (Tmax=788C), alkaliphiles (pHmax 12), ac- oanaerobacterium and a few Thermoanaerobacter species).
idophiles (growing below pH 4), moderate halophiles and The reduction of nitrate to nitrite or ammonia (many fac-
psychrophiles. The traditional designation of lactic acid ultative and strict anaerobes), sulfate to sulfide (Des-
bacteria includes several genera not clustered closely to- ulfotomaculum and related taxa), sulfite and sulfur to
gether phylogenetically (distributed over both phyla), but sulfide, fumarate to succinate, iron(III) to iron(II) (Car-
often considered together in texts, and includes species boxydothermus ferrireducens and probably others, depend-
from the genera Streptococcus, Lactococcus, Lactobacillus ing upon conditions), halogenated aromatic and aliphatic
and Leuconostoc. Two other genera within the Firmicutes compounds to less toxic products (Desulfitobacterium
are Listeria and Caryophanon, which are motile by species) and carbon dioxide to acetate (Moorella therm-
peritrichous flagella and widely distributed in decaying oautotrophica). The acetogenic bacteria can combine both
matter and animal dung. See also: Acidophiles; Alkali- energy-producing strategies when grown heterotrophically
philes; Extreme Thermophiles; Extremophiles; Halophiles; on glucose. The Embden–Meyerhof and then the Wood–
Nitrogen Fixation; Psychrophiles and Psychrotrophs Ljungdahl pathways are employed. These pathways in-
Adenosine triphosphate (ATP) formation is generally volve the formation of tetrahydrofolate derivatives as in-
via substrate level phosphorylation – using energy- termediates to convert the previously formed hydrogen and
rich compounds such as acetylphosphate and phos- carbon dioxide to a third molecule of acetate. This yields
phoenolpyruvate as donors for transferring a phosphate the highest amount of energy observed for the
group to adenosine diphosphate (ADP) and mainly met- anaerobic Gram-type positive bacteria, i.e. five ATP per
abolites, as electron acceptors. The reducing equivalents hexose. ATP can also be formed in Clostridium symbiosum,
formed during oxidation of substrates are transferred to Acidaminococcus fermentans and Propiogenium modestum,
metabolites, producing reduced fermentation products. for example, by the use of sodium ion translocation via
These organisms often utilize the Embden–Meyerhof– decarboxylases and proton-translocating ATP synthases.
Parnass pathway as a basic starting point for the metab- See also: Acetogenic Bacteria; Anaerobic Respiration;
olism of sugars, and the different fermentation pathways DNA Repair
are variants depending upon which metabolite is used as
electron acceptor. ATP yields are two ATPs from the con-
version of hexoses to pyruvate, and up to two additional
ATP via substrate-level phosphorylation with the resultant
Class Mollicutes: Mycoplasmas and
pyruvate. There are a myriad of fermentation pathways Relatives
which may be utilized: the simplest of these is homolactic
acid fermentation (used by Lactobacillus) in which lactate Based on 16S rRNA sequence analysis, the mycoplasmas
dehydrogenase reduces pyruvate to lactate, followed by the (class Mollicutes) have evolved from the clostridia or a
ethanol fermentation typified by Thermoanaerobacter common ancestor. These bacteria are often traditionally
ethanolicus. Other important pathways include the hetero- grouped as ‘other’, and discussed either separately or along
lactic and bifido fermentations of the lactic acid bacteria, with the chlamydiae and rickettsiae (although these Gram-
yielding one and 2.5 ATPs per hexose, respectively; the two type negative bacteria are distinct in being obligate
propionic acid pathways mentioned previously; the but- intracellular parasites). These smallest bacteria capable of
anol–acetone pathway of Clostridium acetobutylicum; and self-reproduction are free-living organisms with no cell

8 ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net
Gram-type Positive Bacteria

wall. Thus, they are pleomorphic in shape although some of the Prokaryotes, http://141.150.157.80/bergeysoutline/
have a special intracellular pseudoskeleton. Mycoplasmas outline/bergeysoutline_5_2004.pdf] Micrococcineae of
require sterols for growth, which they incorporate into Subclass V (including genera such as Micrococcus, Art-
their cell membranes for strength and osmotic stability hrobacter and Kocuria) and several families of suborder
(Prescott et al., 1996). There are currently six genera of the Corynebacterineae (e.g. genus Corynebacterium) produce
only family Mycoplasmataceae within this class, and in- no spores at all. But members of the family Nocardiaceae
clude the genera Ureaplasma, Spiroplasma and Anaero- from the same suborder grow in short aerial and substrate
plasma. However, further molecular investigations may hyphae, which fractionate into many small cells during
produce phylogenetic shifts in the future. Most of these stationary growth phase. The Suborder VIII Actinomyce-
bacteria are quite difficult to grow in culture, owing to tales contain the large genus Actinomyces, whose members
stringent nutritional requirements, and are usually grown produce aerial and substrate mycel-forming hyphae form-
within eukaryotic cells. ing conidia spores. Thus, in traditional texts, many of the
taxa have often been erroneously associated with the
eukaryotic fungi, but the 16S rRNA analysis clearly places
The Phylum Actinobacteria (Class them into the Gram-type positive bacterial phylum Ac-
Actinobacteria) tinobacteria (Embley and Stackebrandt, 1994). There is a
wide variety of spore morphology, from forming a single
The phylum is also called the ‘high G+C branch’. Phylum spore on a sporophore to multiple spores on a sporophore
BXIV Actinobacteria presently contains – despite their ob- or in a sporangium depending on the order and family.
vious physiological and morphological diversity – only one Suborder XIV Streptomycineae contains one of the largest
class, the Actinobacteria. However, five subclasses are con- genera, the genus Streptomyces with presently over 600
tained within the one class. The largest of the five, the species (some of them are and will be reclassified into
Subclass V Actinobacteridae, contains two important or- different genera), and also forms conidiospores. The mor-
ders: the large Order I Actinomycetales with nine suborders phology varies from straight sporophores to coiled and
and over 80 genera, and the Order II Bifidobacteriales highly branched straight or coiled sporophores. Members
which contains the lactate producing Bifidobacteria of the genus Actinoplanes, for instance, produce multiflag-
(Figure 2b). The latter order differs from the homo- and ellated motile actinospores in a sporangium after the
heterolactic acid bacteria, in the order Lactobacillales hyphae has branched within the sporangium. In contrast,
(a Firmicutes), by its members using a special fermentation members of the genus Streptosporangium produce nonmo-
pathway, the so-called bifido-pathway. The Bifidobacteri- tile spores in a sporangium without branching of the
ales are presently of interest as probiotic remedies. See also: hyphae. Many are primarily soil inhabitants with impor-
Actinomycete Spores tance in the mineralization of organic matter and are free-
Members of this phylum are characterized by the high living, although some are pathogenic to other organisms.
(460 mol%) G+C content of their DNA, and are mainly See also: Streptomycete Spores
isolated from terrestrial soil (although recently marine An interesting suborder of the Actinobacteria is
species were isolated). They are primarily aerobic bacteria Suborder XVI, the Frankineae. They contain the N2-
with a few exceptions, e.g. the Propionibacteriaceae and fixing genera Frankia and Blastococcus and in a separate
Bifidobacteriaceae and also Actinomyces bovis, the bovine family the highly radiation-resistant Kineococcus, rival-
pathogen after which the group ‘actinomycetes’ derives its ling the g ray resistance of Deinococcus (Phillips
name. They are all, more or less, pleomorphic ranging from et al., 2002).
slightly pleomorphic rods of the Corynebacteriaceae (con- The mycobacteria belong to the Suborder X [Bergey’s
tains the cellulolytic, motile rod Cellulomonas), to coc- Taxonomic Outline of the Prokaryotes, http://141.150.
ci)rod)cocci changes during a growth cycle of members 157.80/bergeysoutline/outline/bergeysoutline_5_2004.pdf]
of the genus Arthrobacter, to larger mycelia forming cul- Corynebacterineae and are members of the only genus in
tures of the Actinomycetes. Many members play important the family Mycobacteriaceae, genus Mycobacterium. They
roles in biotechnological industrial research. Examples are typically cluster together with members of the families Co-
the members of: the Streptomyces (family Streptomyceta- rynebacteriaceae, Dietziaceae and Nocardiaceae. They are
ceae) with more than 600 described species, and the a medically important group of bacteria, which, as the
Micromonospora (family Micromonosporaceae of the Sub- name implies, were once seen to have ‘fungal’ character-
order XV Micromonospoarideae) which are some of the istics. Their cell envelope structure is typically Gram-type
most important and prolific producers of secondary met- positive, but the production of characteristic waxes pre-
abolites, e.g. important antibiotics, antitumour com- vents the uptake of the primary stain during the Gram
pounds and amino acids. staining procedure. It has long been recognized that these
Similar to the situation of the Firmicutes, in organisms will take up carbol fuchsin dye when heated
respect to endospore formation, there is great gently, then resist decolorizing by acid alcohol – hence their
variety in the phylum Actinobacteria in regard to traditional moniker of ‘acid-fast’. Their cell envelope struc-
spores and resting cell formation. For example, ture severely affects transport of nutrients and other chem-
members of the Suborder IX [Bergey’s Taxonomic Outline icals, one factor which is presumed to make these

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 9
Gram-type Positive Bacteria

organisms (1) slow-growing (doubling times of up to sev- utilized by aerobic organisms which can shuttle the large
eral weeks), (2) quite resistant to killing by host immune amounts of reduced co-factors to the electron transport
mechanisms and antibiotics and (3) difficult to diagnose. chain to generate ATP with molecular oxygen as the final
Members of the genus Corynebacterium are mor- electron acceptor. Even anaerobes contain most of the en-
phologically similar to the skin-dwelling species of Pro- zymes of this cycle but may use an incomplete cycle (lacking
pionibacterium (Suborder XII), such that the latter, which succinate dehydrogenase) to generate carbon skeletons for
are normal human skin flora, have traditionally been biosynthesis, especially a-ketoglutarate and oxaloacetate.
known as coryneforms, or diphtheroids, owing to their re- See also: Citric Acid Cycle; Glycolytic Pathway
semblance to the agent of diphtheria (Corynebacterium The Firmicutes are – although with a few exceptions –
diphtheriae). In the last decade, placement of species within bifurcated in respect to obligately aerobic and obligately
both of these genera has undergone, and is still undergoing, anaerobic (including oxygen tolerant anaerobes, i.e. not
much change. See also: Fungal Cells being able to use oxygen as terminal electron acceptor) and
Suborder XII contains the majority of propionibacteria Actinobacteria are, to a larger extent, aerobic microorgan-
(using lactate and sugars as substrates and producing pro- isms with only a few obligate (oxygen tolerant) anaerobes
pionate and acetate) but also the bifidobacteria (producing such as the Bifidobacteriales and Propionibacterineae.
lactate and acetate). There are actually several genera Anaerobic Gram-type positives can utilize two major
within the so-called propionibacteria, which are especially routes of energy metabolism: substrate-level phosphor-
important in the dairy industry as they produce the char- ylation-based fermentation and electron transport phos-
acteristic flavour and holes of Swiss cheese via their fer- phorylation-based anaerobic respiration. Some bacteria
mentation products propionate and carbon dioxide, can take advantage of both, even within one metabolic
respectively. These include Clostridium propionicum and pathway, e.g. the succinate pathway in propionibacteria or
Megasphaera elsdenii (both within the Firmicutes) and the homoacetogenic pathway of the homoacetogenic
many species in the genus Propionibacterium (within the Firmicutes (see later), whereas other taxa are restricted to
phylum Actinobacteria), of which P. freudenreichii is the one or the other. See also: Anaerobic Respiration; Bacterial
type species. Propionate is mainly formed via two path- Fermentation
ways, the acrylate pathway and the succinate pathway,
named for the primary intermediate in each. Both path-
ways include the formation of acetate as the oxidized Medical Aspects
product which leads to ATP formation (Gottschalk, 1986).
Propionibacteria play an important ecological role by their The Gram-type positive bacteria have medical importance
utilization of the reduced fermentation product lactate, as pathogens, normal flora and producers of antibiotics.
and reduce it further to propionate, with concomitant for- Staphylococcus epidermidis and Lactobacillus vaginalis are
mation of acetate and carbon dioxide. They play a key role key members of the first line of defence against mucocu-
in degradation pathways in anaerobic sewage sludge. The taneous infection in humans, and some Propionibacterium
bifidobacteria are important in the food industry and as species, as well as several staphylococci, are also normal
inhabitants of skin and mucosal surfaces of warm-blooded skin flora. Overall, the mucocutaneous surfaces of most
animals. The bifidobacteria involve an unusual fermenta- warm-blooded animals abound with Gram-type positive
tion pathway, leading to the formation of lactate and ac- bacteria, usually in a protective or commensal relationship.
etate in a 1:1 ratio, and producing acetoin and diacetyl However, there is a fine line between normal flora and
(responsible for ‘buttery’ taste) from side reactions. pathogen with other host defences playing important roles
See also: Bacterial Fermentation in the prevention of potential diseases these ‘normal flora’
can cause. In the modern age of medicine, the phenomenon
of immunosuppression is quite common, as better tech-
Physiological Diversity nology and care extend the lives of persons with inborn and
acquired immune deficiencies. Thus, organisms usually
As partly discussed earlier, the diversity of metabolic path- considered nonpathogenic (in fact, any microorganism)
ways within the Gram-type positive bacteria accounts for can be seen causing unusual and often life-threatening
many of their uses in industry and research. In general, the infections in this population. In the case of Gram-type
aerobes and anaerobes can be considered separately to ex- positive bacteria, this is especially true of the normal
plore these anabolic and catabolic pathways. The aerobic skin flora, certain members of the mycobacteria and
Gram-type positive bacteria generally utilize glycolysis, the the actinomycetes. See also: Infections in the Im-
tricarboxylic acid (TCA) cycle and electron transport for munocompromised Host
production of ATP. Most are capable of utilizing the
Embden–Meyerhof–Parnass pathway and, in part, the Pathogens
pentose phosphate shunt (important for nucleic acid bio-
synthesis), but the Entner–Doudoroff pathway is found The staphylococci and streptococci contain a number of
only among Enterococcus species, being more commonly pathogens that cause skin and soft-tissue infections, such
used by Gram-type negatives. The TCA cycle is generally as cellulitis, impetigo, erysipelas, necrotizing fasciitis,

10 ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net
Gram-type Positive Bacteria

pharyngitis, otitis media and sinusitis. Streptococcus pneu- The mycobacteria contain two well-recognized patho-
moniae is one of the leading causes of pneumonia, along gens: Mycobacterium tuberculosis is the agent of tubercu-
with Gram-type negatives and anaerobes, and is also the losis, and Mycobacterium leprae is the agent of leprosy.
second major cause of bacterial meningitis in adults. The Both are difficult to treat and difficult and time-consuming
highly virulent Streptococcus pyogenes causes the acute to culture for diagnosis or study, in part due to the slow
pharyngitis known as ‘strep throat’ with its characteristic metabolism and antibiotic-resistance offered by their
epidemic nature. Most infected skin wounds involve either unique envelope structure. Other mycobacteria have gen-
staphylococci, streptococci, or both. See also: Bacterial erally been considered nonpathogenic but can cause dis-
Antibiotic Resistance; Bacterial Meningitis; Staphylo- ease in the immunocompromised, with the same problems
coccal Sepsis: Treatment of diagnosis and treatment as their more well-known rel-
Both genera also produce a variety of toxins, causing atives. C. diphtheriae is the cause of diphtheria, now almost
scarlet fever, rheumatic fever, staphylococcal scalded skin unheard of in industrialized countries owing to an effective
syndrome and toxic shock syndrome. Staphylococci are toxoid vaccine (usually administered in combination with
notorious for being resistant to regular penicillins, and the tetanus vaccine). Propionibacterium acnes may be the
many streptococci are becoming similarly resistant. A se- causative agent of acne. See also: Immunodeficiency;
rious dilemma in medicine is Staphylococcus aureus resist- Tuberculosis
ance even to antistaphylococcal penicillins – the so-called The actinomycetes contain genera that are able to infect
methicillin-resistant S. aureus, or MRSA, which is only the skin, sweat glands and lymph systems of mammals,
susceptible to the expensive and toxic intravenous anti- although they usually do so with low incidence and low
biotic vancomycin. MRSA is increasingly common as virulence. As one might expect, these diseases are often
an agent of osteomyelitis, endocarditis and nosocomial diagnosed as fungal, and misguided treatment with anti-
(hospital-acquired) infections, and vancomycin-resistant fungal agents can allow patients to worsen before the cor-
strains have been encountered. Lateral transfer of resist- rect diagnosis is made. Since they are often seen in the
ance genes to other species is quite possible. See also: immunocompromised population, this adds more diffi-
Antibiotic Resistance Plasmids in Bacteria; Toxin Action: culty to management.
Molecular Mechanisms; Toxic Shock Syndrome
Many species of Clostridium produce toxins capable of
causing human disease. Clostridium perfringens is the agent Spoiling Organisms
of classical gas gangrene, and Clostridium tetani produces
the toxin which causes tetanus. A toxoid vaccine has been The resistance of endospores to heat, desiccation and other
successful in combating this often-fatal disease, but it is still physical stressors has allowed organisms that form them to
a major killer in certain areas of the world. Wound or um- become problematic in food production, handling and
bilical stump contamination by this sporulating, anaerobic storage. Spoilage of canned foods that have been heated
soil-dweller can lead to a disease produced by the neuro- and vacuum packed is seen with the anaerobes, which
toxin, which causes unremitting muscle spasms known as produce gases or organic acids by fermentative metabo-
tetany. Wound botulism is another often-fatal condition lisms. Well-recognized for ‘swelled-can’ spoilage is
that is caused by several types of toxin produced by the Thermoanaerobacterium (basonym Clostridium) thermos-
various strains of Clostridium botulinum, collectively re- accharolyticum, which can produce carbon dioxide pres-
ferred to as ‘botulinum toxin’. Clostridium difficile is a mi- sure of several atmospheres within sealed cans (Hollaus
nor member of normal large intestine flora in humans but is and Sleytr, 1972). Another example is Desulfotomaculum
able to overgrow when major genera are killed, such as nigrificans, a thermophilic sulfate-reducer, which produces
during treatment with broad-spectrum antibiotics. It can large amounts of sulfide. While these organisms do not
then produce large amounts of its enterotoxin, which manufacture toxins or act as pathogens, they none the less
causes a clinical syndrome of intractable secretory diar- make foods inedible.
rhoea and intestinal mucosal lesions known as pseudo- Several Gram-type positive bacteria are responsible for
membranous colitis. See also: Botulinum Toxin; food poisoning, i.e. produce a toxin that causes disease
Vaccination upon ingestion of contaminated food. Staphylococcal food
Bacillus anthracis is the agent of the toxin-mediated dis- poisoning is caused by a heat-stable enterotoxin that dis-
ease anthrax. Its natural host is cattle, and awareness of this rupts the function of intestinal mucosal cells, and is pro-
disease and its prevention limit human infections. But as it duced by certain strains of S. aureus growing in improperly
is a sporulating organism and its toxin is quite potent, it is cooked or stored foods. Since it does not produce noxious
important in consideration of biological terrorism or war- gases or odorous organic acids, these contaminated foods
fare. Listeria species are responsible for infant pneumonias appear normal until the rapid onset of symptoms occurs.
and some cases of food poisoning. Mycoplasma species Botulism is most commonly acquired by ingestion of the
cause many cases of so-called ‘walking pneumonia’ in hu- previously mentioned botulinum toxin produced by the
mans, known more properly as atypical pneumonias (other various strains of C. botulinum, whose endospores are al-
cases are caused by viruses and chlamydiae), and myco- lowed to germinate in food as a result of insufficient cook-
plasmas can also cause urinary tract infections. ing. In infant botulism, endospores or vegetative bacteria

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 11
Gram-type Positive Bacteria

on surfaces (rattles, toys, skin, etc.) or in foods (honey occurs via acetate. See also: Bacterial Ecology; Halophiles;
usually contains this bacterium) may grow in the immature Soils and Decomposition; Thermophiles
intestine owing to lack of stomach acid and normal gut Only a small percentage of bacterial species are currently
flora, producing toxin as it does so. The toxin causes a known to us, most growing at or near human body temper-
flaccid paralysis which is fatal in one-third of cases. How- ature, pH and salinity ranges, which reflects our bias towards
ever, the botulinum toxin has also been used since the early studying those organisms directly affecting our health. In-
1980s to treat muscle disorders, e.g. lazy eye and uncon- vestigation into more diverse and extreme habitats will
trolled blinking. Its use by dermatologic surgeons under the undoubtedly lead to the discovery of many more unusual
name Botox for cosmetic use was approved in 2002 by the organisms. Interest in nutrient cycling and bioremediation
U.S. Food and Drug Administration. Bacillus cereus is a will expand our knowledge of bacteria relative to these
sporulating, enterotoxin-producing bacterium with a pro- areas, which may also shed more light on the evo-
clivity for cooked rice dishes. C. perfringens strains can lutionary pathway(s) of this group. See also: Bioremediation
produce an enterotoxin when spores are activated by in-
sufficient cooking of foods and allowed to germinate in the
intestines after being eaten. Cooking of foods to adequate
temperatures and for sufficient times to kill both vegetative Biotechnological Aspects of Firmicutes
bacteria and endospores, proper food storage and avoid- and Actinobacteria
ance of certain foods during infancy can prevent most
Gram-type positive bacterial food poisonings. In the food industry, the lactic acid and propionic acid
producing bacteria are important in the production of
cheeses, fermented meats, pickles, sauerkraut, sourdoughs,
yogurt, fruit juices and other foods, too diverse to be cov-
Habitats and Ecology ered here in detail. Silage, used as stock feed, is produced by
the actions of bacteria on grasses and grains, which in-
Two major habitats support the majority of the Gram-type creases the nutrient value of the grasses. A good number,
positive bacteria: the soil and sediments, and the mucocu- but not all, of these bacteria are Gram-type positive.
taneous surfaces of warm-blooded animals. Much of the Alcohol production still generally utilizes eukaryotic yeasts
bulk of soil microorganisms is within this group, and even for bioproduction, but many anaerobic Gram-type posi-
the characteristic odour of moist earth is predominantly tive bacteria are able to produce ethanol as well, and have
due to the production of volatile substances (such as geos- certain advantages over yeasts for production (Wiegel,
min) by streptomycetes. Extreme environments are well- 1980). Mutant strains of Corynebacterium glutamicum are
colonized by members of the Firmicutes, which can grow at used for the production of L-lysine and other amino acids
temperatures up to 788C (Thermoanaerobacter therm- for use as nutritional supplements and flavourings
ohydrosulfuricus) or down to 2108C (Bacillus psych- (Eggeling, 1994). See also: Mutations and the Genetic Code
rophilus), and pHs as high as 12 or above (some Long known for their medical importance are several
mesophilic Bacillus spp.), and 11.1 at 558C (Clostridium antibiotic-producing species of Streptomyces, which make
paradoxum) or as low as 3.5 (Lactobacillus acidophilus). antifungals such as amphotericin B and nystatin, as well as
Marine as well as freshwater sediments abound with these antibacterial compounds such as cephalosporins, chlo-
bacteria, many of which can tolerate high salinity, e.g. the ramphenicol, erythromycin, neomycin, streptomycin and
Halanaerobiales, are found in salt ponds and natural salt tetracycline. The ability of bacteria to kill each other by the
brines. Thus, as a group, they are ubiquitous due to the fact production of toxins is a crucial area of study for the iso-
that they form heat- and dry-resistant spores or cysts. lation of natural antibiotics, as well as the formulation of
However, some species are indeed ubiquitous whereas oth- synthetic ones. Gram-type positive bacteria are important
ers are defined to specific environments, e.g. C. paradoxum both as sources of this information and as targets whose
is only found in sewage sludge but never in fresh or marine demise is desired. Bacillus species produce bacitracin,
water. While members can be saprophytic or parasitic, polymyxin and gramicidin, which are antibacterial
most are free-living. In their natural habitats, Gram-type (Safiyazov and Mannanov, 1997), as well as a natural in-
positive bacteria have important ecological roles: many are secticide, i.e. the protein toxin crystal made in the parasp-
able to perform denitrification (Micrococcus) and sulfate oral body of Bacillus thuringiensis. Upon ingestion by
reduction (Desulfotomaculum). The chemolithoautotro- certain insects, this toxin crystal undergoes chemical
phic species are valuable since they make nutrients avail- changes which produce damage to the midgut and death
able for the rest of the soil community. The acetogenic to the insect. The toxin is especially effective in the cater-
anaerobes, such as Clostridium formicoaceticum, are a ma- pillar stage of certain moths and butterflies, and molecular
jor source of acetate (which they can form via reduction of technology has been used to insert the toxin genes into
carbon dioxide or via homoacetogenic fermentation of plants to produce insect resistance.
sugars). It is estimated that about three-quarters of the Clostridium acetobutylicum and Leuconostoc mesentero-
methane production in nature by methanogenic archaea ides have been used industrially for butanol production for

12 ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net
Gram-type Positive Bacteria

fuel and the production of dextran, respectively. Several of Boone DR, Liu Y, Zhao Z-J et al. (1995) Bacillus infernus sp. nov.,
the propionic acid bacteria have been used commercially to an Fe(III)- and Mn(IV)-reducing anaerobe from the deep ter-
produce large amounts of vitamin B12 and vitamin K restrial subsurface. International Journal of Systematic Bacte-
(Gardner and Champagne, 2005). Study of their metabolic riology 45: 441–448.
pathways has provided insight into the functions of these Bozzola J and Russell L (1992) The past, present, and future of
vitamins in humans. Bacillus subtilis is widely used in ge- electron microscopy. In: Electron Microscopy, p. 4. Boston,
netic and molecular study and has provided valuable in- MA: Jones and Bartlett.
sights into Gram-type positive bacterial molecular Brill JA and Wiegel J (1997) Differentiation between spore-
mechanisms, such as the complex and widely investigated forming and asporogenic bacteria using a PCR and Southern
hybridization based method. Journal of Microbiological Methods
process of endosporulation. The clostridia are used as
31: 29–36.
model organisms for the study of anaerobic metabolisms.
Collins MD, Lawson PA, Willems A et al. (1994) The phylogeny
Bioremediation continues to receive increasing attention
of the genus Clostridium: proposal of five new genera and eleven
for decreasing pollution in more ecologically sound ways. new species combinations. International Journal of Systematic
Natural dehalogenation and denitrification are performed Bacteriology 44: 812–826.
by certain aerobic and anaerobic Gram-type positive bac- Eggeling L (1994) Biology of L-lysine overproduction by Coryne-
teria (Wiegel et al., 1999). Investigation into the use of mi- bacterium glutamicum. Amino Acids 6: 261–272.
croorganisms as biosensors is a relatively new field in which Embley TM and Stackebrandt E (1994) The molecular phylogeny
Gram-type positive bacteria may play some role. See also: and systematics of the actinomycetes. Annual Review of Micro-
Bioremediation biology 48: 257–289.
Engle M, Li Y, Rainey F et al. (1996) Thermobrachium celere gen.
nov., sp. nov., a rapidly growing thermophilic, alkalitolerant,
Conclusion and proteolytic obligate anaerobe. International Journal of Sys-
tematic Bacteriology 46: 1025–1033.
The Gram-type positive bacteria are a diverse group of Gardner N and Champagne CP (2005) Production of Propioni-
organisms with a wide range of habitats, metabolic capa- bacterium shermanii biomass and vitamin B12 on spent media.
Journal of Applied Microbiology 99: 1236–1245.
bilities and human interactions and consist of two major
Gottschalk G (1986) Bacterial Metabolism, 2nd edn, pp. 242–245.
phyla, the Firmicutes (also called low G+C mol% bacte-
New York: Springer.
ria) and the phylum Actinobacteria (also called high
Gram C (1884) Über die isolierte Färbung der Schizomyceten in
G+C, 455 mol% of the DNA bases guanine and cyto- Schnitt- und Trockenpräparaten. Fortschritte der Medizin 2:
sine, bacteria). Their original distinction by a simple stain- 185–189.
ing reaction has been confirmed to a large extent by recent Hollaus F and Sleytr U (1972) On the taxonomy and fine structure
molecular methods to represent true phylogenetic related- of some hyperthermophilic saccharolytic clostridia. Archiv für
ness, and to define a coherent group of bacteria. Their value Mikrobiologie 86: 129–146.
in medicine, industry and food processing, as well as food Merchante R, Pooley HM and Karamata D (1995) A peri-
spoilage, makes their continued scientific study a must for plasm in Bacillus subtilis. Journal of Bacteriology 177:
practical as well as purely scientific purposes. Changes in 6176–6183.
their classification and nomenclature, as presently for all Mesbah N, David M, Hedrick B et al. (2007) Natranaerobius
bacteria and archaea, are ongoing and likely to continue thermophilus gen. nov., sp. nov., a halophilic, alkalithermo-
to be so for some time. Using the distinction of Gram-type philic bacterium from soda lakes of the Wadi An Natrun, Egypt
(a phylogeny-based systematic term), as opposed to and proposal of Natranaerobiaceae fam. nov. and Natranae-
Gram stain or Gram reaction (a staining reaction-based robiales ord. nov. International Journal of Systematic and
taxonomic term), and clearly delineating which meaning is Evolutionary Microbiology 57: 2507–2512.
being used, will serve to decrease confusion in communi- Murray RGE (1984) The higher taxa, or a place for everything _?
cation regarding some organisms, whose placement in In: Holt JG (ed.) Bergey’s Manual of Systematic Bacteri-
classification schemes is currently unclear. Thus, the au- ology, vol. 1, pp. 31–34. Baltimore, MD: Williams and Wilkins.
thors suggest the use of the terms Firmicutes and Actino- O’Brien JR and George NM (1997) A Gram stain paradox:
Bacillus circulans misidentified as Pseudomonas paucimobilis.
bacteria instead of Gram (type) positive bacteria.
American Journal of Medical Science 18: 111–115.
Onyenwoke RU, Brill JA, Farahi K and Wiegel J (2004) Sporulat-
References ion genes in members of the low G+C Gram-type positive
phylogenetic branch (Firmicutes). Archives of Microbiology
Angert ER, Brooks AE and Pace NR (1996) Phylogenetic analysis 182: 182–192.
of Metabacterium polyspora: clues to the evolutionary origin of Onyenwoke RU and Wiegel J (2008) Genus I. Thermoanaerobac-
daughter cell production in Epulopiscium species, the largest ter. Genus VIII Thermoanaerobacterium. In: Bergey’s Manual
bacteria. Journal of Bacteriology 178: 1451–1456. of Systematic Bacteriology. Springer Verlag: New York-
Beveridge TJ and Schultze-Lam S (1996) The response of selected Heidelberg (in press).
members of the Archaea to the Gram stain. Microbiology 142: Phillips RW, Wiegel J, Berry CJ et al. (2002) Kineococcus
2887–2895. radiotolerans sp. nov., a radiation-resistant, gram-positive

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 13
Gram-type Positive Bacteria

bacterium. International Journal of Systematic and Evolu- Wiegel J (1980) Formation of ethanol by bacteria. A pledge for the
tionary Microbiology 52: 933–938. use of extreme thermophilic bacteria in industrial ethanol fer-
Popescu A and Doyle RJ (1996) The Gram stain after more than a mentation processes. Experientia 36: 1434–1446.
century. Biotechnic and Histochemistry 71: 145–151. Wiegel J (1981) Distinction between the Gram reaction and the
Prescott L, Harley J and Klein D (1996) The bacteria: remaining Gram type of bacteria. International Journal of Systematic Bac-
Gram negative bacteria and cyanobacteria. In: Microbiology, teriology 31: 88.
3rd edn, p. 45. Dubuque, IA: WC Brown. Wiegel J (2007) Family Clostridiaceae. In: Bergey’s Manual of
Rainey F, Tanner R and Wiegel J (2006) An introduction to Systematic Bacteriology. Springer: New York (in press).
the family Clostridiaceae. In: Dworkin M, Falkow S, Wiegel J and Adams MWW (eds) (1998) Thermophiles: The Keys
Rosenberg E, Schleifer K-H and Stackebrandt E (eds) The to Molecular Evolution and the Origin of Life? London: Taylor
Prokaryotes. A Handbook on the Biology of Bacteria, vol. 4. and Francis.
Bacteria: Firmicutes, Cyanobacteria, pp. 650–673. Berlin: Wiegel J and Quandt L (1982) Determination of the Gram type
Springer. using the reaction between polymyxin B and lipopolysaccha-
Safiyazov JS and Mannanov RN (1997) Biochemical analysis of rides of the outer cell wall of whole bacteria. Journal of General
antibiotic production by endophytic and soilborne strains of Microbiology 128: 2261–2270.
Bacillus subtilis. Seventeenth International Congress of Bio- Wiegel J, Zhang X and Wu Q (1999) Anaerobic dehalogenation of
chemistry and Molecular Biology, San Francisco, CA. August hydroxylated polychlorinated biphenyls by Desulfitobacterium
24–29. FASEB Journal 11: A1216. dehalogenans. Applied and Environmental Microbiology 65:
Schleifer KH and Kandler O (1972) Peptidoglycan types of bac- 2217–2221.
terial cell walls. Bacteriological Reviews 36: 407–477. Williams ST, Locci R, Beswick A et al. (1993) Detection and
Scott JR and Barnett TC (2006) Surface proteins of gram-positive identification of novel actinomycetes. Research in Microbiology
bacteria and how they get there. Annual Review of Microbiology 144: 653–656.
60: 397–423. Woese C, Kandler O and Wheelis M (1990) Towards a natural
Siunov AV, Nikitin DV, Suzina NE et al. (1999) Phylogenetic system of organisms: proposal for the domains Archaea, BAC-
status of Anaerobacter polyendosporus, an anaerobic, poly- TERIA, and EUKARYA. Proceedings of the National Acad-
sporogenic bacterium. International Journal of Systematic Bac- emy of Sciences of the USA 87: 4576–4579.
teriology 49: 1119–1124.
Takai K, Inoue A and Horikoshi K (1999) Thermaerobacter Further Reading
marianensis gen. nov., sp. nov., an aerobic extremely therm-
ophilic marine bacterium from the 11 000 m deep Mariana Balows A, Trüper HG, Dworkin M, Harder W and Schleifer K-H
Trench. International Journal of Systematic Bacteriology 49: (eds) (1992) The Prokaryotes, 2nd edn. New York: Springer.
619–628. Caldwell DR (1995) Microbial Physiology and Metabolism.
Vreeland RH and Rosenzweig WD (2002) The question of Dubuque, IA: WC Brown.
uniqueness of ancient bacteria. Journal of Industrial Microbi- Garrity GM (ed.) (2001, 2005) Bergey’s Manual of Systematic
ology and Biotechnology 28: 32–41. Bacteriology, 2nd edn. New York: Springer.

14 ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net

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