Вы находитесь на странице: 1из 7

Bacterial Ecology

Tom Fenchel, University of Copenhagen, Helsingr, Denmark

Bacterial ecology is concerned with the interactions between bacteria and their environments and with the role of bacteria in biogeochemical element cycling.

Secondary article
Article Contents
. Introduction . Habitats for Bacterial Growth . Physiological Limits . Roles of Bacteria in Nature

Concepts and methods of bacterial ecology are strongly avoured by the small size of bacteria, by their apparent omnipresence, and by their metabolic diversity. Bacteria (in this article dened as all prokaryotes thus including eubacteria as well as archaebacteria or archaea) represent the earliest known type of life and their presence at least 3.5 109 years ago is well documented. All basic properties of element cycling in the biosphere had developed before multicellular eukaryotes (algae, plants, fungi and animals) evolved perhaps about 6 106 years ago. Even in the extant biosphere bacteria play a dominating role as agents of chemical transformations. Although methods of molecular genetics have recently made it possible to study the phylogenetic relationship between dierent taxonomic groups of bacteria and to condently identify a given strain of bacterium, there is still no precise denition of what constitutes a bacterial species. Bacteria are sexless (although horizontal gene transfer may take place even between dierent species) and so a biological species concept is not applicable. A pragmatic approach has been to dene a species by its particular combination of phenotypic traits: only about 5000 species have until now been named in this way. Many more, however, have not yet been characterized in pure cultures or may still be undiscovered. On the other hand, there is no biogeography of bacteria: it is presumed that a given bacterial species will always occur wherever its specic environmental requirements are found.

. Bacterial Symbioses

Habitats for Bacterial Growth

Bacteria are almost omnipresent, but they do have one absolute requirement for metabolic activity and growth: liquid water. While bacteria are important in terrestrial habitats, their activity is conned to water lms within soil particles or on the surfaces of litter and plants. In terrestrial habitats bacteria have rivals as decomposers of organic material in the form of fungi that are more tolerant to water stress. Many soil bacteria have special adaptations for withstanding water stress such as the formation of (desiccation resistant) endospores (Bacillus, Clostridium), polymorphic life cycles (Myxobacteria), and, in some forms, mycelial growth mimicking the fungi (Actinomy-

cetes). Special bacterial biota occur in the root zone (rhizosphere) of vascular plants; the bacteria utilize dissolved organic matter that leaks from roots. The water column of lakes and seas typically contain between 105 and 107 bacterial cells per millilitre of water, corresponding to a biovolume comparable to that of other, larger plankton organisms. The bacteria metabolize dissolved organic matter; this nourishment derives from algal exudation, lysing protists and animals, and from terrestrial run o. In part, special bacterial biota are associated with suspended, nonliving organic particles (marine snow); bacterial mucous secretions constitute a part of these suspended particles and contribute to their growth through agglutination with other particles. The upper layers of aquatic sediments contain bacterial densities that are two to three orders of magnitude higher than those in the water column. The bacterial biota are also more complex because the bulk of the sediments constitutes an anaerobic habitat. Electron acceptors for bacterial respiration are provided from above through molecular diusion. Thus, oxygen is quickly depleted in the uppermost part of the sediment and other electron acceptors 2 2 , Mn4 1 , Fe3 1 , SO2 (NO3 4 ) are used by dierent types of anaerobic bacteria; when all these electron acceptors have been depleted, terminal mineralization is due to methanogenesis (Figure 1). Many bacteria tend to attach (permanently or temporarily) to solid surfaces. In aquatic environments surfaces are quickly covered by biolms consisting of bacterial cells and their mucous secretions (often together with various unicellular eukaryotes). In the absence of animals that graze or otherwise disturb biolms these may develop into microbial mats. Hot springs of geothermal origin and salterns (evaporation ponds for salt production) harbour cyanobacterial mats; the dominating process is oxygenic photosynthesis carried out by cyanobacteria, but a great variety of other functional types of bacteria are present. Cyanobacterial mats may eventually grow to a thickness of several centimetres or even metres (stromatolitic mats) although almost all biological activity is conned to the uppermost millimetres (Figure 2). Similar, albeit short-lived and much less impressive mats may occur on sediments in the intertidal zone. Mass occurrences of photosynthetic purple sulfur bacteria are often seen during summer where

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

Bacterial Ecology



NO3 Depth in sediment

N2 CO2

Mn4+, Fe3+ (CH2O) Fermentation Fatty acids, H2, alcohols

Mn2+, Fe2+ CO2





Figure 1 A simplified presentation of the vertical zonation of microbial respiration processes in an aquatic sediment. [CH2O] represents organic matter. In the oxic surface layer degradation takes place by oxygen respiration, which prevails because it is the energetically most favourable process. Since the vertical transport of oxygen is due to molecular diffusion it is quickly depleted, sometimes less than 1 2 mm beneath the surface. Other terminal electron acceptors then take over in a succession that reflects the descending energy yield of the involved respiration processes. In marine sediments sulfate reduction predominates quantitatively due to 2 the high concentration of SO2 in seawater; in other systems 4 methanogenesis plays an important role.

Extreme environments, in which animals, algae, and sometimes even unicellular eukaryotes are absent, may still support bacterial biota. In addition to hyperthermal and hypersaline habitats, these include extremely acid (mine drainages) and alkaline (soda lakes) waters. Recently, bacterial biota have been found in subsurface environments hundreds of metres below the ground surface; in some cases evidence suggests that these biota cannot have had surface contact for 4 106 years (Ghiorse, 1997). Most subsurface bacteria seem to subsist mainly by metabolizing hydrogen and assimilating carbon dioxide. Finally, many bacteria live in facultatively or obligatory symbiotic relationships with dierent protists, animals or plants. The signicance of these symbiotic relationships is not always understood, but in many cases these are clearly adaptive to the hosts. Conversely, probably all animal and plant species may fall victim to a variety of more or less seriously pathogenic bacteria.

Figure 3 Mass occurrence of purple sulfur bacteria on the top of decaying seaweeds in a shallow bay. These photosynthetic bacteria depend on light and on sulfide as a reductant.

Figure 2 A vertically cut slice of a 7 mm thick cyanobacterial mat. The green colour of the top millimetre is due to filamentous cyanobacteria (the darker green towards the bottom part of this layer reflects higher pigment contents caused by exposure to lower light intensities). White carbonate precipitations are seen beneath the green layer. The purple colour of the middle part of the mat is due to photosynthetic purple bacteria; below them a green-brown colour discloses the presence of green sulfur bacteria.

decomposing seaweeds accumulate in shallow water (Figure 3). White mats of colourless sulfur bacteria (basing their energy metabolism on the oxidation of sulde with O2 2 or NO3 ) may cover the sea oor in productive sites in shallow water (Figure 4) or in deeper waters where the overlying water column has a very low oxygen content. Mats of chemolithotrophic sulfur bacteria also occur around hydrothermal vents.

Figure 4 The filamentous colourless sulfur bacterium Beggiatoa on the top of a sandy sediment (individual sand grains measure about 200 mm). A few colonies of the purple sulfur bacterium Thiocapsa are also visible.

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

Bacterial Ecology

Physiological Limits
The ecological role of bacteria can be understood only from their physiological properties. Many traits (e.g. tolerance to environmental variables, metabolic requirements) are primarily studied in pure cultures. However, bacteria do not live in isolation from other species in nature and interactions between dierent physiological types of bacteria represent an essential feature of microbial communities.

The adaptive signicance of motility is that bacteria can orient themselves in gradients of attractant or repellent chemical solutes (chemotaxis) or light (phototaxis); thus bacteria are able to migrate towards more benign microhabitats.

The ability to live in extreme environments is a distinctive property of bacteria. Many bacteria are quite specialized with respect to their environment, but taken together, bacteria represent tolerance limits that far exceed what can be found among eukaryotes. Anaerobiosis is perhaps not an extreme environment in this context. Anaerobic microhabitats abound in aquatic habitats and a great variety of anaerobic bacteria exist. Mineralization is predominantly anaerobic in aquatic sediments, in waterlogged soil particles, and in several other habitats, and many essential biogeochemical transformations take place only under anaerobic conditions. Anaerobic bacteria may be facultative; that is, they are capable of oxygen respiration, but can complete their life cycle using an alternative (anaerobic) type of energy metabolism. Obligate anaerobes are incapable of using oxygen and strict anaerobes are also extremely sensitive to oxygen: even trace levels below those detectable by ordinary analytical methods may inactivate or kill these forms. More surprising is the ability of some specialized forms to thrive at temperatures exceeding 808C, or 4 1008C at hyperbaric pressures (extreme thermophiles), in saturated brine (extreme halophiles), and acidophiles and alkalophiles live at pH values below 2 and exceeding 10, respectively. Under less extreme environmental conditions it is also possible to identify dierent bacterial strains that thrive only within more or less narrow intervals of temperature, salinity, etc. Psychrophilic bacteria thrive at low temperatures and some may grow at subzero temperatures, for example, in sea ice.

General properties of bacteria especially related to small size

Typical bacteria measure 12 mm in length and the smallest free-living species measure around 0.5 mm; a few species (mainly among cyanobacteria and chemolithotrophic sulfur bacteria), are considerably larger (up to 80 mm has been reported; a recently discovered sulfur bacterium, Thiomargarita, may obtain a diameter of up to 0.3 mm). Single cells may have spherical, cylindrical or helical shapes. Many bacteria form (mainly lamentous) colonies. The small size of bacteria means that they have high volume-specic metabolic and growth rates. Thus, some bacteria may divide (double their biomass) every 20 minutes. In nature, growth rates may be considerably lower due to dierent limiting factors (temperature, availability of substrates), but even so, doubling times are usually measured in hours. A relatively small bacterial biomass will therefore be responsible for relatively high rates of chemical transformations and ows of energy. Transport of solutes to the cells takes place only through molecular diusion and at low substrate concentrations diusive ux to the cells constitutes the rate-limiting factor for metabolic activity. In contrast to eukaryotic cells, bacteria do not have a cytoskeleton and are instead almost always surrounded by a rigid cell wall. As a consequence, bacteria can only incorporate low-molecular weight solutes from the surroundings. When bacteria utilize polymers (such as polysaccharides or proteins) these must rst be hydrolysed by extracellular (membrane-bound) hydrolytic enzymes before the resulting monomers can be brought into the cells. The transport of monomers into the cells may take place through passive (facilitated diusion) or active (energy-requiring) transport. Bacteria are extremely eective at exploiting very dilute solutions; this is basically a function of their small size and so they are superior competitors (relative to the usually much larger eukaryotic cells) in utilizing dissolved substrates. Many bacteria are motile. Bacteria swim using one or several rigid, helix shaped, rotating agella. Velocities attained are typically about 50100 mm s 2 1, but some are faster. Other bacteria (many lamentous and some noncolonial forms) show gliding motility on solid surfaces.

Metabolic diversity
Many bacteria are very specialized regarding types of substrates they can exploit and the type of energy metabolism they can apply. Taken together, however, bacteria represent a great diversity in this respect. The principal types of bacterial energy metabolism are shown (somewhat simplied) in Table 1. It is noteworthy that the dierent processes are often interdependent in nature. Phototrophic and oxidative sulde oxidations, for example, require the production of sulde; this is provided by sulfate reducers. The complete fermentation of carbohydrates (to acetate plus hydrogen) is thermodynamically possible only at a very low ambient hydrogen tension. Certain types of fermenting bacteria therefore live in close physical proximity to hydrogen-scavenging bacteria (methanogens, sulfate reducers) that in turn depend on

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

Bacterial Ecology

Table 1 Principal types of bacterial energy metabolism Fermentation: Anaerobic processes involving the dismutation of (organic) molecules; no external electron acceptor. Low energy yields. Metabolites include various low molecular weight organic compounds (alcohols, fatty acids) and hydrogen. Complete fermentation to acetate plus hydrogen requires a low ambient hydrogen tension. Respiration: Aerobic respiration: oxidation of substrates with oxygen. Organotrophs oxidize organic matter; principal metabolites carbon dioxide and water. Carried out by a large number of aerobic bacteria that dier (among other properties) with respect to which polymers they can hydrolyse. Specialized aerobes, the chemolithotrophs, oxidize inorganic substrates. Nitriers 1 2 2 2 to NO3 (via NO2 ); colourless sulfur bacteria oxidize H2S to So and SO2 oxidize NH4 4 , and methanotrophs oxidize CH4. Many bacteria catalyse the oxidation of reduced iron and manganese; energy conservation from this process has not been demonstrated in all cases. Anaerobic respiration: use of external electron acceptors other than oxygen. In most cases the involved species can use only a limited number of low molecular organic compounds in addition to hydrogen. They thus depend on metabolites of 2 fermenting bacteria. Denitriers use NO3 and produce N2 (and some other N compounds) as metabolites. Sulfate reducers 22 use SO4 and produce H2S. Manganese and iron reducers use Mn4 1 and Fe3 1 to produce Mn2 1 and Fe2 1 , respectively. Methanogenesis: Methanogens produce CH4 from CO2 1 H2 or by dismutation of acetate into CO2 1 CH4. Some methanogens can also use reduced C1 compounds (e.g. methanol) to produce CH4. Phototrophy: Oxygenic photosynthesis occurs in cyanobacteria. Light energy is harvested to reduce carbon dioxide to organic matter, using water as reductant and producing oxygen as a metabolite. Anoxygenic photosynthesis implies the use of reductants other than water (primarily H2S, H2 and Fe2 1 ). Occurs among several bacterial groups such as in, for example, purple and green sulfur bacteria.

the hydrogen production of fermenting bacteria. This interspecies hydrogen transfer is an example of syntrophy: bacteria with complementary types of metabolism are interdependent and always occur together in natural microbial communities. Organotrophic bacteria are specialized with respect to the types of polymers they can hydrolyse. Under aerobic conditions probably all naturally occurring (and many xenobiotic) compounds can be utilized by at least some species. Cellulose and other polysaccharides are degraded quickly (also under anaerobic conditions) while other polymers (lignin, phenols, cork substances) are degraded very slowly. Hydrocarbons (including crude oil) can be degraded both aerobically and anaerobically (by sulfate reducers). Under anaerobic conditions primary degradation of polymers is predominantly due to fermenting bacteria, since most anaerobic respirers and methanogens use only low-molecular weight compounds (notably fatty acids, alcohols and hydrogen) that are fermentative metabolites. Certain polymers do not seem to be easily broken down under anaerobic conditions (e.g. lignin) so that wood is often preserved in anoxic sediments. Anaerobic degradation may stall if conditions acidify; this happens in moors and results in peat formation; over geological time and through abiological processes peat transforms into lignite and eventually coal. Humic acids

are believed to consist mainly of lignin residues; their microbial degradation is a very slow process. In organotrophs assimilatory carbon metabolism is usually supplied by the same organic compounds that serve for dissimilatory (energy) metabolism. Autotrophic bacteria must cover their carbon demand through (energyrequiring) assimilatory reduction of carbon dioxide. Similarly, many bacteria are capable of assimilatory 2 2 and SO2 as sources for organic reduction of NO3 4 nitrogen and sulfur. During the degradation of mineralpoor organic substances (wood, straw) bacteria must assimilate inorganic nitrogen and phosphorus, thus eectively competing with plants for these nutrients. Nitrogen xation is an assimilatory process that occurs exclusively in some bacteria. It is an anaerobic process and the ability to x nitrogen is especially common among anaerobes and microaerophiles; it also occurs among some aerobes (many cyanobacteria, Azotobacter, Rhizobium) that have special adaptations to protect the nitrogenase complex from oxygen exposure.

Roles of Bacteria in Nature

The fundamental and unique roles of bacteria in nature are (1) as links in food chains between detritus (including

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

Bacterial Ecology

dissolved organic matter) and bacterivorous protozoa and animals, (2) their dominance as mineralizers of organic carbon, and (3) catalysis of essential chemical processes in the biosphere. In the extant biosphere the most important primary producers are constituted by vascular plants (on land) and by algae (in the sea). Photosynthesis results in a chemical disequilibrium (reduced carbon plus oxygen). Bacteria are the main players in re-establishing chemical equilibrium: due to spatial and temporal heterogeneities, transport limitation and kinetic constraints these mineralization processes are complex and they drive the major biogeochemical cycles of carbon, nitrogen, and sulfur.

Food chain

Dissolved organic compounds Primary producers Particulate detritus Bacteria

Bacteria as primary producers

In certain environments, especially in nutrient-depleted oceanic waters, unicellular cyanobacteria play a substantial role as primary producers as compared to eukaryotic algae. Colonial lamentous cyanobacteria may temporarily play a similarly important role in shallow seas and in lakes; the capability of nitrogen xation renders cyanobacteria superior competitors among phototrophs when waters become depleted in reactive nitrogen, but when phosphate is still available. Other types of bacterial autotrophs are, of course, also primary producers in the sense that they assimilate carbon dioxide to produce organic substances. However, the energy needed for this process (typically in the form of reduced inorganic compounds such as, for example, hydrogen sulde) originally derives from plant tissue that has been degraded under anaerobic conditions. In a biosphere context, these organisms then rather exemplify the complexities of mineralization processes. Chemoautotrophic bacteria associated with hydrothermal vents depend on substrates (sulde, methane) deriving from geothermal processes; again, however, these resources can only be exploited in the presence of oxygen that originally derives from photosynthesis.

Figure 5 The microbial loop: in most ecological systems a substantial fraction of the primary production is first degraded by bacteria. In the process bacterial biomass is generated and this enters the food chains, typically via bacterivorous protozoa.

containing) end products of anaerobic degradation such as methane or hydrogen sulde. Conversely, bacteria are capable of degrading all naturally occurring polymers and they can assimilate dissolved inorganic nutrients from the environment. They are extremely ecient in assimilating dissolved organic material, converting it into particulate food that is available to phagotrophs. Also, specialized chemolithotrophic bacteria can harvest the energy of, for example, dissolved sulde to produce bacterial cells. Bacteria thus play an essential role as food chain links between primary production and animals.

Biogeochemical cycling
Bacteria constitute the most important agent for the mineralization of organic carbon in almost all natural ecosystems. In this context a number of essential processes in the biosphere are exclusively catalysed by bacteria. One such example is the generation of methane (by methanogenic bacteria in certain anaerobic habitats; some atmospheric methane, however, also derives from geothermal processes in the Earths crust) and the re-oxidation of methane by other types of bacteria in aerobic environments such as soils (some methane oxidation also takes place through photochemical processes in the upper part of the atmosphere). Bacteria also transform and control concentrations of a number of other atmospheric trace gases (Conrad, 1996). The global nitrogen cycle provides an example of the importance of bacterial processes. Atmospheric nitrogen is made available to the biota through bacterial nitrogenxation (some nitrogen is oxidized in the atmosphere during electric discharges; the resulting nitrogen oxides are also available as nitrogen sources for the biota). In living tissue nitrogen occurs in a reduced form and it is excreted mainly as ammonia. The dissimilatory re-oxidation of

Bacteria as links in food chains

A large part of the primary production (in many ecological systems it is by far the largest fraction) is not consumed directly by animals. Rather, the organic material is degraded by bacteria. Bacteria are then consumed by protozoa or microscopic animals that again serve as food for larger animals (Figure 5). The concept has been referred to as the microbial loop (in the context of plankton food chains, but it applies equally well to other ecosystems). There are several reasons for this: animals are in general incapable of hydrolysing most polymeric plant compounds and most plant tissue is very poor in essential nutrients, e.g. nitrogen and phosphorus. Finally, animals are not capable of utilizing dilute solutions of organics, nor the (energy-

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

Bacterial Ecology

ammonia to nitrate is a bacterial process. So is dissimilatory denitrication; its principal product is nitrogen, and this represents the only mechanism by which atmospheric nitrogen is replenished. Bacteria play a substantial and often unique role for a number of other biogeochemical processes, including the oxidation and re-oxidation of metals, dissimilatory sulfate reduction and sulde oxidation, and carbonate deposition and dissolution.

Bacterial Symbioses
Many examples of symbiotic bacteria within or on animals, plants and protists have been described. Among them many are poorly understood while others have been studied extensively due to their great economic signicance. The following refers mainly to such well-studied cases.

Symbiotic nitrogen fixation

While free-living nitrogen-xing bacteria occur it is believed that by far the largest share of terrestrial nitrogen xation takes place in symbiotic relations with plants. The process requires anaerobic conditions and substantial amounts of energy; both conditions can be provided by plant hosts. The best known, and economically most important example is the symbiosis of Rhizobium in members of the Leguminosae. Most legumes host more or less specic strains of the bacterium. Rhizobium occurs naturally in soil, and especially in the rhizosphere of legumes. Infection of the host plants takes place via root hairs. The bacteria invade root cells and form nodules; they then transform into swollen bacterioids. The bacterioids x nitrogen and feed the host plant with nitrogen in the form of ammonia; in return the host provides carbon substrates for the bacteria. A special feature is the presence of a haemoglobin (which is jointly synthesized by the bacterium and the host plant). It secures an almost anaerobic environment while at the same time supplying oxygen for bacterial metabolism. A number of other such symbioses are known: several woody angiosperms (including, for example, alder and sweet gale) harbour the nitrogen-xing bacterium Frankia in root nodules. Other plants harbour cyanobacterial symbionts (cycads, the water fern Azolla); these symbioses also are important for their nitrogen xation.

of anaerobic bacteria that ferment polysaccharides into low molecular fatty acids; these are then assimilated by the animal. Ruminants (and kangaroos and a few other types of herbivorous mammals) have pregastric fermentation. In cows and sheep, the rumen is anatomically a part of the oesophagus and it constitutes 1015% of the volume of the animal. The rumen is a fermentation chamber containing a consortium of anaerobic bacteria that ferment cellulose, xylan, pectins and starch (but not lignin) into acetate, butyrate and propionate. The concomitant hydrogen production is consumed by methanogenic bacteria and the cow rids itself of methane through belching. The fatty acids are absorbed and they constitute the carbon source for the host. Microbial cells are subsequently digested in the true stomach and constitute the sole protein source for the host animal. Excreted urea is recycled via saliva as a nitrogen source for the microbial biota. Adult ruminants are entirely dependent on their microbial symbionts. Other mammals (horses, elephants, rodents, lemurs, etc.) have postgastric fermentation: food is rst subject to acid digestion in the stomach and indigestible components are subsequently fermented in a caecum associated with the hindgut. Symbiotic polymer degradation occurs less frequently among nonmammalian animals; it has been reported from a few species of birds, reptiles and sh. Among invertebrates it has been found in certain sea urchins and shipworms; termites have symbiotic cellulose degradation, but in most termite groups the principal cellulose decomposers are eukaryotic microorganisms.

Other examples of bacterial symbioses

Many other kinds of bacterial symbioses exist; these are generally of no or little economic signicance and appear more exotic. Many marine benthic invertebrates harbour symbiotic chemolithotrophic bacteria. These are mainly colourless sulfur bacteria although two cases of methaneoxidizing symbionts have also been found. Such symbioses have recently been found to occur within several groups of bivalves, polychaetes, oligochaetes, nematodes, and in all pogonophorans. The symbionts are situated in the gills (bivalves), on the body surface or in special organs. The hosts supply the symbionts with a suitable mixture of oxygen and sulde through dierent mechanisms. The symbionts are either digested by the host or they excrete dissolved organic matter that can be utilized by the hosts. Some species have become entirely dependent on the symbionts and are gutless. These symbioses were rst studied in detail in hydrothermal vent faunas, but have since been recorded in many common shallow-water species (Southward, 1987). Some species of squids and sh harbour bacteria that confer luminescence on their hosts. Some organisms use bacterial symbionts as tools of biological warfare such as

Symbiotic polymer degradation

Many herbivores, especially mammals belonging to dierent taxa, have solved the problem of low nitrogen and phosphorus contents in their food and the inability to utilize structural plant polymers by hosting a consortium

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

Bacterial Ecology

the symbionts of certain strains of the ciliate Paramecium: when the bacteria are released in the water they kill other, competing Paramecium strains. Certain nematodes kill their insect prey by injecting them with pathogenic bacteria. Some bacterial symbionts seem to play a role in the biosynthesis of necessary growth factors; thus certain trypanosomes (parasitic agellates) require a symbiont bacterium for the synthesis of haem. A large number of other symbioses that seem to be specic and essential to their hosts have been described, but their true adaptive signicance remains to be discovered.

Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO2, CH4, OCS, N2O, NO). Microbiological Reviews 60: 609640. Ghiorse WC (1997) Subterranean life. Science 275: 789791. Southward EC (1987) Contribution of symbiotic chemoautotrophs to the nutrition of benthic invertebrates. In: Sleigh MA (ed.) Microbes in the Sea, pp. 83118. New York: Wiley.

Further Reading
Armitage JP and Lackie JM (eds) (1990) Biology of the Chemotactic Response. Cambridge: Cambridge University Press.

Balows A, Tru per HG, Harder W and Scheifer K-H (eds) (1991) The Prokaryotes, vols 14, 2nd edn. New York: Springer. Edwards C (ed.) (1990) Microbiology of Extreme Environments. New York: McGraw Hill. Fenchel T, King GM and Blackburn TH (1998) Bacterial Biogeochemistry. The Ecophysiology of Mineral Cycling, 2nd edn. San Diego, CA: Academic Press. Fenchel T and Finlay BJ (1995) Ecology and Evolution in Anoxic Worlds. Oxford: Oxford University Press. Fletcher M, Gray TRG and Jones JG (eds) (1987) Ecology of Microbial Communities. Cambridge: Cambridge University Press. Ford TE (ed.) (1993) Aquatic Microbiology. An Ecological Approach. Oxford: Blackwell. Hobson PN (ed.) (1989) The Rumen Microbial Ecosystem. London: Elsevier. Koch AL (1990) Diusion. The crucial process in many aspects of the biology of bacteria. Advances in Microbial Ecology 11: 3770. Lengeler JW, Drews G and Schlegel HG (1999) Biology of the Prokaryotes. Stuttgart, Germany: Georg Thieme Verlag. Madigan MT, Martinko JM and Parker J (1997) Biology of Microorganisms, 8th edn. Upper Saddle River, NJ: Prentice Hall. Postgate J (1982) The Fundamentals of Nitrogen Fixation. Cambridge: Cambridge University Press. Smith DC and Douglas AE (1987) The Biology of Symbiosis. London: Edward Arnold. Tate RL (1995) Soil Microbiology. New York: Wiley.

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net