Trichomonads

Secondary article

Nigel Yarlett, Pace University, New York, USA

Article Contents
. Introduction

Trichomonads are flagellate protozoa that contain an intracellular fibrous rod composed of
thousands of microtubules termed the axostyle.

. Brief Description and Characterization

. Taxonomic Classification of the Trichomonads
. Major Subtaxa

Introduction

. Phylogenetic and Evolutionary Considerations

Trichomonads are agellate protozoa that inhabit the

alimentary canal or urogenital system of vertebrates and
invertebrates. They include the urogenital parasites,
Trichomonas vaginalis and Tritrichomonas foetus, which
are the causative agents of human and bovine trichomoniasis, respectively. Other representatives are parasites of
birds; e.g. Trichomonas gallinae is a pathogen of Colombian and galliform birds, which invades tissues of the head,
neck, brain and viscera.

cytoskeletal structures by connecting the kinetosomes to

one another and to other parts of the cell (Honigberg and
Brugerolle, 1989). The majority of trichomonads examined
to date contain electron-dense microbody-like organelles
termed paraxostylar or paracostal granules because of
their close association with these structures (Figure 2).
These organelles play an important role in trichomonad

Brief Description and Characterization

The following is a general description of the order.
Trichomonads are variable in size, ranging from 5 to 25
 2.5 to 12.5 mm. The body is usually pyriform, with a
rounded anterior end and a pointed posterior end (Figure 1).
There is a single nucleus in the anterior part of the body.
Anterior to the nucleus is a blepharoplast composed of
several kinetosomes, which gives rise to three to ve
anterior agella, and in some species a posterior or
recurrent agellum. The recurrent agellum is anchored
dorsal to the anterior locomotor organelles and is
incorporated into the undulating membrane. The undulating membrane extends from the anterior end about one
half to two thirds of the cell length. In some species the
recurrent agellum extends beyond the undulating membrane as a free agellum.
A rod-like axostyle arises from the blepharoplast,
passing through the centre of the cell and emerging from
the posterior end. The anterior part of the axostyle is
enlarged, forming the capitulum in which the nucleus sits.
The capitulum is continuous with the pelta, forming the
peltaaxostylar complex, a crescent-shaped membranous
structure consisting of two microtubular sheets. This
structure has a supportive role, reinforcing the wall of the
periagellar canal. The costa, the largest rootlet organelle,
arises from the blepharoplast and is thought to support the
overlaying undulating membrane. Its presence dierentiates the family Trichomonadidae from other parabasilids.
Dorsal to the nucleus is found the parabasal apparatus;
this typically V-shaped structure is composed of a
parabasal body and two parabasal laments. The parabasal laments or lamellae are proposed to function as

Figure 1 Scanning electron micrograph of dorsal (left) and dorsolateral

(right) views of Trichomonas vaginalis. Characteristic structures include four
anterior flagella (AF). The recurrent flagellum (RF) can be seen emerging
from the periflagellar canal (PC). The margin of the undulating membrane
(UM) is typically shorter than the body and consists of the attached part of
the recurrent flagellum and the outer accessory filament. The axostyle (A) is
well developed and extends beyond the posterior end of the cell. Bar, 5 mm.
(Reproduced with permission from BM Honigberg (ed.) (1989)
Trichomonads Parasitic in Humans. New York: Springer-Verlag.)

ENCYCLOPEDIA OF LIFE SCIENCES 2001, John Wiley & Sons, Ltd. www.els.net

Trichomonads

dae and Calonymphidae. Assignment is based upon the

number and length of anterior agella, the presence or
absence of an undulating membrane or recurrent agellum, the size and shape of the axostyle and costa.

Major Subtaxa
Family: Trichomonadidae

Figure 2 Transmission electron micrograph of Trichomonas vaginalis.

Section through the anterior part of the organism showing the Golgi
apparatus (G), a hydrogenosome (H), the axostyle (A), and the costa (C).
(Courtesy of Dr M. Vannier-Santos, Universidade Federal do Rio de Janeiro,
Brazil.)

metabolism and were subsequently renamed hydrogenosomes, based upon biochemical function. Typical subcellular structures such as rough endoplasmic reticulum
(surrounding the nucleus), Golgi apparatus, lysosomes
and glycogen granules are visible in transmission electron
micrographs of thin sections (Figure 2).

Taxonomic Classification of the

Trichomonads
Kingdom: Protista
Subkingdom: Dimastigota
Superphylum: Tetramastigota
Phylum: Axostylata
Class: Parabasalea
Order: Trichomonadida
Trichomonads are classied as parabasilids, in the
phylum Axostylata (Lee et al., 1985) which includes all
protozoa possessing an intracellular rod composed of
thousands of microtubules, termed the axostyle. This
structure primarily had a role in cell motility, and skeletal
roles were later evolutionary adaptations. The parabasilids
are a heterogeneous class, but they all contain parabasal
bodies, which are aggregates of very large dictyosomes
with kinetosome-associated bres. Typical mitochondria
are absent, but all representatives possess hydrogenosomes, which are believed to be divergent mitochondria.
The parabasilids can be endozoic, feeding on bacteria and
particulate material. They have representatives that are
important pathogens of humans and higher animals. The
order Trichomonadida encompasses four families the
Trichomonadidae, Monocercomonadidae, Devescovini2

The Trichomonadidae is divided into four subfamilies

(Table 1), three of which have representatives that are
parasitic in humans and higher animals. The subfamily
Trichomonadinae comprises four genera (Table 1) which
are characterized by the presence of an undulating
membrane that is bordered by a agellum. The axostyle
often conspicuously protrudes from the posterior end, and
the costa is well developed and associated with hydrogenosomes. This subfamily contains the genus Trichomonas (Donne), which includes some of the most studied
species of trichomonads. Microscopically the genus
Trichomonas is distinguishable from the other members
of this subfamily by the absence of a free posterior
agellum and the presence of an undulating membrane,
which is shorter than the body (Figure 1, Table 1). Other
distinguishing features include a relatively slender costa
and a spatulate axostylar capitulum, which is of moderate
width and connects to the slender pelta. The trunk of the
axostyle is slender; and the parabasal body is rod- or Vshaped, with either one or several laments (Honigberg
and Brugerolle, 1989). Included in this genus is Trichomonas vaginalis, a parasite responsible for human trichomoniasis, a frequently encountered sexually transmitted
disease. In common with other trichomonads, T. vaginalis
possesses hydrogenosomes (Figure 2) which act as redox
organelles in an analogous manner to the mitochondria of
aerobic cells. They are microaerophilic, with an optimal
requirement of 5 0.25 mmol L 2 1 oxygen, which is
comparable to the vaginal oxygen concentration. Another
notable species is T. tenax, a commensal of the human oral
cavity, which is distinguished by the absence of axostyleassociated hydrogenosomes (paraxostylar granules),
although costa-associated hydrogenosomes are present
(paracostal granules). T. gallinae is an oral pathogen of
birds, which can cause a fatal disease in young pigeons.
The genus Trichomitus (Swezy) is distinguished from
other members of Trichomonadinae by the variable length,
height and number of undulations of the undulating
membrane. The costa is slender and weakly developed in
most, and the capitulum of the axostyle has conspicuous
ventrolateral extensions. Typical representatives include
T. batrachorum, present in the large intestine of amphibians and reptiles, and T. rotunda found in the pig intestine
(Lee et al., 1985).

Trichomonads

Table 1 The family Trichomonadidae

Subfamily

Species

AF

UM

PF

PB

Host

Trichomonadinae

Trichomonas vaginalis
Trichomitus batrachorum
Tetratrichomonas prowazeki
Pentatrichomonas hominis
Tritrichomonas foetus
Tritrichomonas augusta
Tritrichomonas muris
Trichomitopsis termopsidis
Pseudotrypanosoma giganteum
Pentatrichomonoides scroa

4
3
4
5
3
3
3
4
4
5

S
V
B
B
B
B
B
B
B
S

0
F
F
F
F
F
F
F
0
0

r/v
v
d
e
r
r
r
r
b
e

Human
Amph/rep
Amph/rep
Mammals
Cattle
Reptile
Mouse
Termite
Termite
Termite

Tritrichomonadinae

Trichomitopsiinae
Pentatrichomonoidinae

AF, anterior agellum; UM, undulating membrane; PF, posterior agellum; PB, parabasal body; S, short; V, variable; B, body length; F, free;
r, rod-shaped; v, v-shaped; d, discoid; e, elliptical; b, band-shaped; Amph, amphibian; rep, reptile.

Members of the genus Tetratrichomonas (Parisi) have a

distinct undulating membrane extending the length of the
body. In T. prowazeki, found in the large intestine of
amphibians and reptiles, the capitulum of the axostyle has
no ventrolateral extensions.
Members of the genus Pentatrichomonas (Mesnil) have
ve anterior agella; four are grouped together at the base
and one is independent. The capitulum of the axostyle has
some ventrolateral extensions, and the parabasal body
appears to be composed of small granules, e.g. P. hominis
found in the large intestine of humans, primates, cats, dogs
and rodents.
The subfamily Tritrichomonadinae contains the genus
Tritrichomonas (Kofoid) which is distinguished by a small
or absent pelta, and a stout tube-like axostyle which
projects from the posterior end with one or more
periaxostylar rings. Included in this genus is T. foetus
(Riedmuller), which causes bovine abortion. T. foetus has
three anterior agella and a free posterior agellum of
equal length. The undulating membrane extends the full
length of the cell and has an accessory lament along its
margin. The costa is prominent, and the axostyle thick with
ventrolateral extensions from the capitulum to the small
pelta. Other representatives of this genus include T.
augusta, present in the large intestine of amphibians and
saurian reptiles (lizards) and T. muris from the mouse
intestine. On the basis of ne structure and isozyme
analysis, it is thought that T. suis found in the pig intestine
is actually a variant strain of T. foetus.
The subfamily Trichomitopsiinae contains species that
have long, band-shaped parabasal bodies with a lament.
Included in this group are the genera Trichomitopsis
(Kofoid and Swezy) and Pseudotrypanosoma (Grassi).
These are distinguished by the presence of a posterior
agellum and an unbranched axostyle in Trichomitopsis,
and the absence of a posterior agellum but the presence of
a branched axostyle in Pseudotrypanosoma.
Members of the Pentatrichomonadinae have ve identical anterior agella, plus a recurrent agellum at the

margin of a low undulating membrane, which spirals

around the body. There is no free posterior agellum. The
axostyle is slender and does not project at the rear. The
parabasal body is elliptical, pyriform or circular. Representatives include P. scroa found in the termite gut.

Family: Monocercomonadidae
The family Monocercomonadidae is represented by
trichomonads with a poorly developed or absent undulating membrane (cresta). Three subfamilies are distinguished
on the basis of the recurrent agellum (Table 2). The
subfamily Monocercomonadinae (Grassi) contains several
genera, which exhibit varying development of the recurrent
agellum from absent to well developed. The genus
Monocercomonas is typied by the presence of a free
recurrent agellum (twice the length of the anterior
agellum), which adheres some distance along the accessory lament. The axostyle is slender and the axostylar
capitulum connects to the pelta. Species are found in the
large intestine and cloaca of snakes, lizards and amphibians.
The genus Tricercomitus has a long free recurrent
agellum (210  body length), with the proximal part
adherent to the dorsum near the posterior end. The
axostyle is slender and barely visible. Tricercomitus is
found exclusively in the termite gut (Lee et al., 1985).
The genus Hexamastix has recurrent agella, which are
approximately the same length as the anterior agella. The
axostyle can be slender or stout, and the axostylar
capitulum connects to the pelta. Hexamastix species are
found in the intestines of caudate amphibians, reptiles and
insects (Lee et al., 1985).
The remaining genera of the Monocercomonadinae
have no recurrent agellum or undulating membrane and
exhibit amoeboid motility. Histomonas has a single
anterior agellum, a small axostyle containing a capitulum, a bilobed parabasal body, which is about the same size
3

Trichomonads

Table 2 The family Monocercomonadidae

Subfamily

Species

AF

UM

RF

Monocercomonadinae

Monocercomonas colubrorum
Tricercomitus termopsidis
Hexamastix batrachorum
Histomonas meleagridis
Dientamoeba fragilis
Chilomitus caviae
Hypotrichomonas acosta

3
3
5
1
0
3
3

0
0
0
0
0
0
S

2 
42
1 
0
0
1 
PF

Chilomitinae
Hypotrichomonadinae

B
 B
B

PB

Host

v/r
d
v/r
bl
b
rg
v/r

Reptile
Termite
Amphibian
Avian
Human
Mammal
Reptile

AF, anterior agellum; UM, undulating membrane; RF, recurrent agellum; PB, parabasal body; S, short; B, body length; PF, posterior
agellum; v, v-shaped; r, rod-shaped; d, discoid; bl, bilobed; b, bean-shaped; rg, ring-shaped.

as the nucleus. H. meleagridis causes a fatal enterohepatitis

(blackhead) of turkeys. Dientamoeba also lacks anterior
agella and an axostyle. D. fragilis, found in the human
intestine, has a bean-shaped parabasal body, which is close
to the nucleus.
The subfamily Chilomitinae is characterized by the
presence of a single recurrent agellum, which originates
from an anterioventral funnel. The axostylar trunk is
slender and does not project from the posterior end.
Chilomitus caviae (da Fonseca) is found in the guinea-pig
intestine.
Members of the Hypotrichomonadinae have a shallow
undulating membrane, a free posterior agellum, and the
costa is absent. The axostylar capitulum has ventrolateral
extensions, which connect to a well-developed pelta.
Representatives are found in the large intestine of reptiles
and land tortoises.

Family: Devescovinidae
Members of the Devescovinidae are characterized by the
absence of an undulating membrane. They typically have
three anterior agella, and the subfamilies are distinguished on the basis of the presence of a true posterior
agellum and axostyle development (Table 3).
Devescovininae representatives have a ribbon-like
posterior agellum and a slender axostyle. There are two
genera, Devescovina and Foaina (Janicki). Devescovina
have a long parabasal body, which wraps around the
nucleus and the axostyle, whereas Foaina have single
parabasal bodies, which are ramied or ring-shaped. The
subfamily Gigantomonadinae, typied by the genus

Gigantomonas (Dogiel), has a long ribbon-like trailing

agellum, which lightly adheres to the body along the edge
of the cresta. The cresta is elongated and forms a large
internal membrane, which may be mistaken for an
undulating membrane. It occurs as a binucleate amoeboid
form during division. Members of the Devescovinidae are
found in the gut of termites (Lee et al., 1985).

Family: Calonymphidae
These are trichomonads with a permanent multinuclear
organization. Each nucleus is associated with a blepharoplast, which is composed of the agella, a parabasal body
and an axial lament. This complex is termed the
karyomastigont, and the complex lacking the nucleus an
akaryomastigont (Lee et al., 1985). There are four genera,
which are distinguished by the development of the
karyomastigont system (Table 4).
Members of the genus Kirbynia (Grasse and Hollande)
have three anterior agella, one posterior agellum and the
parabasal body encircles the nucleus. This genus has a
polykaryomastigont stage and is found in the guts of North
African termites.
Members of the genus Coronympha (Kirby) have 8 to 16
karyomastigonts arranged as a circle at the anterior. There
are three body length agella and a single posterior
agellum per karyomastigont. Members of the genus
Metacoronympha (Kirby) have from 66 to 345 individual
karyomastigonts arranged in a spiral. Both these genera
are found in the guts of South American termites.

Table 3 The family Devescovinidae

Subfamily

Species

AF

UM

PF

PB

Host

Devescovininae

Devescovina vestita
Foaina inata
Gigantomonas herculea

3
3
3

0
0
0

2  B
2  B
42  B

L
rg
L

Termite
Termite
Termite

Gigantomonadinae

AF, anterior agellum; UM, undulating membrane; PF, posterior agellum; PB, parabasal body; B, body length; L, long; rg, ring.

Trichomonads

Table 4 The family Calonymphidae

Species

AF

PF

PB

Host

Kirbynia pulchra
Coronympha octonaria
Metacoronympha senta
Calonympha grassi

3
3/k
3/k
3/k

1
1/k
1/k
1/k

1
816
150
A

sn
sn
sn

Termite
Termite
Termite
Termite

AF, anterior agellum; PF, posterior agellum; K, karyomastigont; PB, parabasal body; A, akaryomastigont; sn, spirals nucleus.

The genus Calonympha (Foa) is akaryomastigont and

represented by species that are found solely in the termite
gut.

Phylogenetic and Evolutionary

Considerations
Molecular phylogeny of the parabasilids
Several molecular and biochemical features have been used
to determine the phylogenetic relationships of the various
orders within the parabasilids and also to determine the
relationships of parabasilids to other protists. Some of the
major phylogenetic markers that have been used are shown
in Table 5 and Table 6. Comparison of partial sequences of
small subunit rRNA (SS-rRNA: Table 5) indicates that
trichomonads diverged at the base of the eukaryotic tree
after the diplomonads and microsporidia but before the
Euglenozoa (Gunderson et al., 1995). This branching order
is upheld using elongation factor-1a and -2 analysis, which
place microsporidia, diplomonads and trichomonads in
order of emergence from the base of the eukaryotic tree.
Traditionally, hypermastigotes were considered to have
arisen from the devescovinids, and the most ancient lineage
of parabasalids was reasoned to be the monocercomonads
based upon cytoskeletal simplicity. Based upon rRNA
analysis, the hypermastigotes branch early but are not
specically related to the devescovinids. Molecular phylogeny based upon the complete 16S-like rRNA sequence
concludes that the Calonymphidae are related to the

Devescovinidae, and with the exception of T. foetus the

Trichomonadidae form a well resolved clade (Silberman
et al., 1996). There appears to be little support for a
preferred branching order between clades for the Trichomonadidae, the Monocercomonadidae, the Calonymphididae or the Devescovinididae using maximum parsimony
and distance methods. Trichomitus trypanoides branches
with T. vaginalis, diering from neighbour-joining analysis
of 28S-rRNA sequences, which place T. batrachorom at the
base of the tree. In general, results of rRNA analysis agree
that the Trichomonadidae share most recent common
ancestry with an unidentied protist from the hindgut of
the termite Reticulitermes avipes (Fukura et al., 1996).
An Entrez search of the GenBank database lists over 160
entire or partial nucleotide sequences that are known for a
representative diversity of the taxa (interested readers are
referred to http://www.ncbi.nih.gov). The protein sequence database, however, predominantly lists sequences
from T. vaginalis. Some of these proteins and their
evolutionary signicance are shown in Table 6. In general,
sequence data for the hydrogenosomal enzymes do not
show a high degree of homology to any of their
mitochondrial equivalent counterparts indicative of the
early branching and long independent evolutionary history
of this group.
Of the cytosolic enzymes sequenced (Table 6), malate
dehydrogenase was found to be distant to the mitochondrial enzyme, once again conrming the ancient lineage of
this group. The glycolytic enzyme, pyrophosphate-dependent phosphofructokinase (ppi-PFK), separated from
other anaerobic protists (Giardia sp. and Entamoeba pf2), and shows the highest degree of homology with ppi-

Table 5 Genomic sequence information

Nucleic acid

Sequence information

LS-rRNA
SS-rRNA
16S-like RNA
23S-rRNA

Trichomonads diverged early preceding the Euglenozoa

Trichomonads diverged after diplomonads and microsporidia
Dientamoeba related to trichomonads. Except for T. foetus, the Trichomonadidae form a well resolved clade
Trichomonads emerged near base of eukaryotic tree. Devescovinidae and Calonymphidae are the earliest
lineages
Hypermastigotes diverge early and are not specically related to the devescovinids
Structurally and functionally similar to initiator elements of higher eukaryotes

rRNA
CPE

LS-rRNA, large subunit-ribosomal ribonucleic acid; SS-rRNA, small subunit-rRNA; CPE, consensus promoter element.

Trichomonads

Table 6 Phylogenetic information deduced from protein sequence information

Protein

LS

Sequence information

PFK
GAPDH
MDH
CP
SOD
Malic enzyme
AK
Ferredoxin
PFOR
Hydrogenase
STK
Val tRNA syn
B DNA polym
RNA polym II
CDC2/28 PK
Cdk
EF 1a and 2
Calmodulin
E-2 ubiquitin
Polyubiquitin
p-Glycoprotein
Actin
HSP70
Cpn60
hyd targ seq
Histones

C
C
C
ly
H
H
H
H
H
H
H
N
N
N
N
C
N
C
N
N
M
M
H
H
C
N

11

Separates from Giardia and Entamoeba. Related to Naegleria ppi-PFK

Separates Trichomonadinae from monocercomonads and T. foetus
Distant to mitochondrial enzyme
Cp1-cp5, belongs to the cathepsin L/cathepsin H/papain family
Clusters with proteobacterial enzymes. Endosymbiont origin
Highly diverged from other malic enzymes
No close association to known AK
Similar to Pseudomonas and Cyanobacteria ferredoxins
Homologous to eubacterial avodoxin enzymes, but not to archaea
*predicted from genomic clones TvhydA and B to have 18 and 7-13 LS
a2b2 protein, evolutionarily equidistant from bacterial and eukaryotic sequences
Clusters with other mitochondrial valyl tRNA synthetases
a, d, e forms present in common with all eukaryotes
a-amantin resistant, lacks 7-peptide repeat of all eukaryotes
Earliest eukaryote reported to possess this feature
T. vaginalis and Giardia exhibit two of the most divergent sequences
Places trichomonad branch after microsporidia and diplomonads
Similar sequence homology with other eukaryotes
Conjugation in place in ancient eukaryotes
Synonymous substitutions present 3 dierent sequences
Single domain unlike later eukaryotes, which are 2 domain
Parabasalids branch above diplomonads
Contains GDAWV signature sequence of mitochondrial HSP70
Similar to mitochondrial Cpn60
Can also target hydrogenosomal proteins into mitochondria
Signicant divergence from other eukaryotes

ND
12
9
8
5
*
9

512

PFK, phosphofructokinase; GAPDH, glyceraldehyde phosphate dehydrogenase; MDH, malate dehydrogenase; CP, cysteine proteinase;
SOD, superoxide dismutase; AK, adenylate kinase; PFOR, pyruvate ferredoxin oxidoreductase; STK, succinate thiokinase; val tRNA syn,
valyl tRNA synthetase; polym, polymerase; PK, protein kinase; Cdk, cyclin-dependent kinase; EF, elongation factor; HSP, heat-shock
protein; Cpn, chaperonin; hyd targ seq, hydrogenosomal targeting sequence; ND, not determined; L, localization; LS, leader sequence; C,
cytosol; H, hydrogenosome; N, nucleus; ly, lysosome; M, plasma membrane fraction; GDAWV, glycine-aspartic acid-alanine-tryptophanvaline.

PFK of the mitochondriate heterolobosean, Naegleria

fowleri (Mertens et al., 1998). Another cytosolic enzyme,
glycolytic glyceraldehyde-3-phosphate dehydrogenase
(GAPDH), showed no homology to the heterolobosean
enzyme and the close relationship of the ppi-PFKs was
probably the result of small sample size. The trichomonad
GAPDH was found to possess a 1011 residue insertion
not found on any other GAPDH (Viscogliosi and Muller,
1998), an unusual property for a cytosolic enzyme.

Mitochondria and hydrogenosomes share a

common origin
Trichomonads are one of the earliest diverging eukaryotic
lineages and occupy a pivotal position in the evolution of
the eukaryotic cell by being the earliest surviving branch to
possess a redox organelle (the hydrogenosome). The
diplomonads (e.g. Giardia sp.) and the microsporidia lack
both hydrogenosomes and mitochondria. The hydrogeno6

some, however, is present in later evolutionary forms such

as rumen holotrich and entodiniomorphid ciliates, certain
free-living sulde ciliates and the rumen fungi. The
organelle therefore appears to be a common feature of
eukaryotes adapted to anaerobic environments. Hydrogenosomes are, however, biochemically distinct in lacking
DNA, cristae, cardiolipin, a tricarboxylic acid cycle, F1F0ATPase and cytochromes. In common with mitochondria
they possess a double membrane and couple pyruvate
metabolism to an electron acceptor, but unlike mitochondria this results in the formation of molecular hydrogen.
ATP is formed by substrate level phosphorylation via
succinate thiokinase, which conserves the high-energy
thioester bond of coenzyme A. Hydrogenosomes have also
been implicated to have a role in calcium storage, much the
same as mitochondria.
Several independent ndings have signicantly revised
our view of the phylogenetic origin of the hydrogenosome,
and also of the age of the mitochondrion, which may have

Trichomonads

arisen several million years earlier than previously

predicted.
Genes for the heat-shock proteins (HSP) involved in
organelle biogenesis, HSP70, chaperonin (Cpn60) and
HSP10, were identied in the nuclear genome of T.
vaginalis. Cpn60 and HSP10 are characteristic of organelles of endosymbiotic origin. Phylogenetic reconstructions placed these sequences unambiguously within the
mitochondrial clade, strongly indicating that trichomonad
genes share a common ancestor with mitochondrial genes,
and strengthens the proposal that mitochondria and
hydrogenosomes share a common ancestor. Further
products of some of these genes were localized in
trichomonad hydrogenosomes using heterologous antibodies to HSP. It is proposed that these proteins
participate in biogenesis of the hydrogenosome as occurs
in mitochondria. This viewpoint is also supported by
several independent molecular studies. Molecular analysis
of the T. vaginalis nuclear valyl tRNA synthetase gene
demonstrates the presence of a high degree of sequence
homology with mitochondrial valyl tRNA synthetases,
suggesting that this mitochondrial gene was transferred to
the trichomonad nucleus (Brown and Doolittle, 1995).
Further evidence that hydrogenosomes and mitochondria share a common ancestor is provided by sequence data
from several hydrogenosomal proteins which all possess a
5 to 12 amino acid extension not found on the native
protein. Six of seven leader sequences begin with Met-LeuSer, and all begin with Met-Leu, and have Arg at position
2 2 from the cleavage site (Lahti et al., 1994). These highly
conserved terminal sequences are similar to mitochondrial
import sequences, and have been shown to be capable of
targeting passenger proteins into mitochondria (Hausler
et al., 1997). Collectively, these data strongly support the
idea that mitochondria and hydrogenosomes share a
common evolutionary ancestor.
Another feature reported in T. vaginalis that is
characteristic of mitochondria-containing eukaryotes is
the presence of the E-2 ubiquitin conjugation pathway
(Keeling et al., 1996). The E-2 ubiquitin conjugation
pathway plays a central role in the conjugation of ubiquitin
to target proteins in several cellular functions including the
degradation of misfolded or short-lived proteins, DNA
repair, cell cycle control and membrane translocation. The
exact function of the E-2 ubiquitin pathway in T. vaginalis
is unknown but the presence of this trait in the early
branching trichomonads is the rst evidence that conjugation machinery was in place during early eukaryotic
evolution (Keeling et al., 1996). The gene for calmodulin
was also recently reported for T. vaginalis. Calmodulin is a
member of a family of high anity calcium-binding
proteins. The trichomonad calmodulin gene was found to
have a high degree of sequence homology to this gene from
mitochondrial-containing eukaryotes and suggests that
calmodulin was a likely feature of the common ancestor of
all extant eukaryotes.

The aforementioned studies strongly support the secondary loss of the mitochondria by trichomonads. Similar
results have been obtained for microsporidia and Entamoeba providing critical evidence that no premitochondrial stage of the eukaryotic cell survived.
The hydrogenosome is not, however, a functionally
impaired mitochondrion. It has acquired proteins not
present in the mitochondrion, in particular, hydrogenase.
The origin of this key hydrogenosomal enzyme has yet to
be determined, but it is clear that the acquisition of this
protein played a major role in the evolutionary transition
of this structure.

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Trichomonads

Further Reading
Biagini GA, Finlay BJ and Lloyd D (1997) Evolution of the
hydrogenosome: mini review. FEMS Microbiology Letters 155: 133
140.
Bui ET, Bradley PJ and Johnson PJ (1996) A common evolutionary
origin for mitochondria and hydrogenosomes. Proceedings of the
National Academy of Sciences of the USA 93: 96519656.
Cavalier-Smith T (1987) The simultaneous symbiotic origin of mitochondria, chloroplasts and microbodies. Annals of the New York
Academy of Sciences 503: 5572.
Horner DS, Hirt RP, Kilvington S, Lloyd D and Embley TM (1996)
Molecular data suggests an early acquisition of the mitochondrion
endosymbiont. Proceedings of the Royal Society of London Series B
262: 10531059.

Karlin S and Brocchieri L (1998) Heat shock protein 70 family: multiple

sequence comparisons, function, and evolution. Journal of Molecular
Evolution 47: 565577.
Muller M (1992) Energy metabolism of ancestral eukaryotes: a
hypothesis based on the biochemistry of amitochondriate parasitic
protists. BioSystems 28: 3340.
Muller M (1997) Evolutionary origins of trichomonad hydrogenosomes:
comment. Parasitology Today 13: 166167.
Roger AJ, Clark CG and Doolittle WF (1996) A possible mitochondrial
gene in the early-branching amitochondriate protist Trichomonas
vaginalis. Proceedings of the National Academy of Sciences of the USA
93: 1461814622.
Sogin ML and Silberman JD (1998) Evolution of the protistan parasites
from the perspective of molecular systematics. International Journal of
Parasitology 28: 1120.