Jan22BacterialEcology.PDF

Bacterial Ecology Tom Fenchel, University of Copenhagen, Helsingør, Denmark Bacterial ecology is concerned with the interactions between bacteria and their environments and with the role of bacteria in biogeochemical element cycling. Introduction 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 de?ned as all prokaryotes thus including eubacteria as well as archaebacteria or archaea) represent the earliest known type of life and their presence at least 3.5C210 9 yearsagoiswelldocumented.Allbasicproperties of element cycling in the biosphere had developed before multicellulareukaryotes(algae,plants,fungiandanimals) evolved perhaps about 6C210 6 years ago. Even in the extantbiospherebacteriaplayadominatingroleasagents ofchemical transformations. Although methods of molecular genetics have recently made it possible to study the phylogenetic relationship between di?erent taxonomic groups of bacteria and to con?dentlyidentifyagivenstrainofbacterium,thereisstill noprecisede?nitionofwhatconstitutesabacterialspecies. Bacteriaaresexless(althoughhorizontalgenetransfermay take place even between di?erent ?species?) and so a biological species concept is not applicable. A pragmatic approach has been to de?ne a species by its particular combinationofphenotypictraits:onlyabout5000species have until now been named in this way. Many more, however, have not yet been characterized in pure cultures ormaystillbeundiscovered.Ontheotherhand,thereisno biogeography of bacteria: it is presumed that a given bacterial species will always occur wherever its speci?c environmentalrequirements are found. 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,theiractivityiscon?nedtowater?lmswithinsoil particlesoronthesurfacesoflitterandplants.Interrestrial habitats bacteria have rivals as decomposers of organic materialintheformoffungithataremoretoleranttowater 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 organicmatter thatleaks fromroots. The water column of lakes and seas typically contain between 10 5 and 10 7 bacterial cells per millilitre of water, correspondingtoabiovolumecomparabletothatofother, 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 growththroughagglutination with otherparticles. Theupperlayersofaquaticsedimentscontainbacterial densities that are two to three orders of magnitude higher thanthoseinthewatercolumn.Thebacterialbiotaarealso morecomplexbecausethebulkofthesedimentsconstitu- tes an anaerobic habitat. Electron acceptors for bacterial respiration are provided from above through molecular di?usion. Thus, oxygen is quickly depleted in the upper- most part of the sediment and other electron acceptors (NO 3 2 ,Mn 41 ,Fe 31 ,SO 4 22 )areusedbydi?erenttypesof anaerobicbacteria;whenalltheseelectronacceptorshave beendepleted,terminalmineralizationisduetomethano- genesis (Figure 1). Manybacteriatendtoattach(permanentlyortempora- rily)tosolidsurfaces.Inaquaticenvironmentssurfacesare quicklycoveredbybio?lmsconsistingofbacterialcellsand their mucous secretions (often together with various unicellular eukaryotes). In the absence of animals that grazeorotherwisedisturbbio?lmsthesemaydevelopinto ?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. Cyanobacterialmatsmayeventuallygrowtoathicknessof several centimetres or even metres (stromatolitic mats) although almost all biological activity is con?ned to the uppermostmillimetres(Figure 2).Similar,albeitshort-lived andmuchlessimpressivematsmayoccuronsedimentsin the intertidal zone. Mass occurrences of photosynthetic purplesulfurbacteriaareoftenseenduringsummerwhere Article Contents Secondary article . Introduction . Habitats for Bacterial Growth . Physiological Limits . Roles of Bacteria in Nature . Bacterial Symbioses 1ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net decomposing seaweeds accumulate in shallow water (Figure 3).Whitematsofcolourlesssulfurbacteria(basing theirenergymetabolismontheoxidationofsul?dewithO 2 or NO 3 2 ) 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 aroundhydrothermalvents. Extreme environments, in which animals, algae, and sometimesevenunicellulareukaryotesareabsent,maystill 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 environ- ments hundreds of metres below the ground surface; in somecasesevidencesuggeststhatthesebiotacannothave hadsurfacecontactfor 410 6 years(Ghiorse,1997).Most subsurfacebacteriaseemtosubsistmainlybymetabolizing hydrogenandassimilatingcarbon dioxide. Finally,manybacterialiveinfacultativelyorobligatory symbiotic relationships with di?erent protists, animals or plants.Thesigni?canceofthesesymbioticrelationshipsis notalwaysunderstood,butinmanycasestheseareclearly adaptivetothehosts.Conversely,probablyallanimaland plant species may fall victim to a variety of more or less seriously pathogenicbacteria. Depth in sediment (CH 2 O) Fermentation Fatty acids, H 2 , alcohols CO 2 Mn 4+ , Fe 3+ Mn 2+ , Fe 2+ CO 2 NO 3 ? N 2 CO 2 O 2 H 2 O CO 2 SO 4 2? H 2 S CO 2 CO 2 CH 4 Figure 1 A simplified presentation of the vertical zonation of microbial respiration processes in an aquatic sediment. [CH 2 O] 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 the high concentration of SO 4 22 in seawater; in other systems methanogenesis plays an important role. 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. 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 4 The filamentous colourless sulfur bacterium Beggiatoa on the top of a sandy sediment (individual sand grains measure about 200mm). A few colonies of the purple sulfur bacterium Thiocapsa are also visible. Bacterial Ecology 2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net Physiological Limits The ecological role of bacteria can be understood only from their physiological properties. Many traits (e.g. tolerance to environmental variables, metabolic require- ments) are primarily studied in pure cultures. However, bacteriadonotliveinisolationfromotherspeciesinnature and interactions between di?erent physiological types of bacteria represent an essential feature of microbial communities. General properties of bacteria ? especially related to small size Typicalbacteriameasure1?2mminlengthandthesmallest free-living species measure around 0.5mm; a few species (mainly among cyanobacteria and chemolithotrophic sulfur bacteria), are considerably larger (up to 80mm has been reported; a recently discovered sulfur bacterium, Thiomargarita, may obtain a diameter of up to 0.3mm). Single cells may have spherical, cylindrical or helical shapes.Manybacteriaform(mainly?lamentous)colonies. The small size of bacteria means that they have high volume-speci?c 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 di?erent limiting factors (temperature, availability of substrates), but even so, doubling times areusuallymeasuredinhours.Arelativelysmallbacterial 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 di?usion and at low substrate concentrations di?usive?uxtothecellsconstitutestherate-limitingfactor formetabolic activity. In contrast to eukaryotic cells, bacteria do not have a cytoskeletonandareinsteadalmostalwayssurroundedby a rigid cell wall. As a consequence, bacteria can only incorporate low-molecular weight solutes from the sur- roundings. When bacteria utilize polymers (such as polysaccharidesorproteins)thesemust?rstbehydrolysed 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 di?usion) or active (energy-requiring)transport.Bacteriaareextremelye?ec- tive at exploiting very dilute solutions; this is basically a function of their small size and so they are superior competitors(relativetotheusuallymuchlargereukaryotic cells) inutilizing dissolvedsubstrates. Many bacteria are motile. Bacteria swim using one or several rigid, helix shaped, rotating ?agella. Velocities attained are typically about 50?100mms 21 , but some are faster. Other bacteria (many ?lamentous and some noncolonialforms)showglidingmotilityonsolidsurfaces. The adaptive signi?cance 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 micro- habitats. Extremophiles Theabilitytolivein?extremeenvironments?isadistinctive property of bacteria. Many bacteria are quite specialized with respect to their environment, but taken together, bacteriarepresenttolerancelimitsthatfarexceedwhatcan 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 water- logged soil particles, and in several other habitats, and manyessentialbiogeochemicaltransformationstakeplace onlyunderanaerobicconditions.Anaerobicbacteriamay be facultative; that is, they are capable of oxygen respiration, but can complete their life cycle using an alternative (anaerobic) type of energy metabolism. Ob- ligate anaerobes are incapable of using oxygen and strict anaerobes are also extremely sensitive to oxygen: even trace levels below those detectable by ordinary analytical methodsmayinactivateorkill these forms. More surprising is the ability ofsome specializedforms to thrive at temperatures exceeding 808C, or 41008Cat hyperbaric pressures (extreme thermophiles), in saturated brine (extreme halophiles), and acidophiles and alkalo- philes live at pH values below 2 and exceeding 10, respectively.Underlessextremeenvironmentalconditions itisalsopossibletoidentifydi?erentbacterialstrainsthat 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,forexample, insea ice. 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 simpli?ed) in Table 1. It is noteworthy that the di?erent processes are often interdependent in nature. Phototrophic and oxidative sul?de oxidations, for exam- ple, require the production of sul?de; this is provided by sulfate reducers. The complete fermentation of carbohy- drates (to acetate plus hydrogen) is thermodynamically possible only at a very low ambient hydrogen tension. Certaintypesoffermentingbacteriathereforeliveinclose physical proximity to hydrogen-scavenging bacteria (methanogens, sulfate reducers) that in turn depend on Bacterial Ecology 3ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net the hydrogen production of fermenting bacteria. This interspecieshydrogentransferisanexampleofsyntrophy: 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 polysaccharidesare 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 degrada- tion of polymers is predominantly due to fermenting bacteria, since most anaerobicrespirers andmethanogens 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. Anaerobicdegradationmaystallifconditionsacidify;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 degradationisa veryslowprocess. In organotrophs assimilatory carbon metabolism is usuallysuppliedbythesameorganiccompoundsthatserve for dissimilatory (energy) metabolism. Autotrophic bac- teria must cover their carbon demand through (energy- requiring) assimilatory reduction of carbon dioxide. Similarly, many bacteria are capable of assimilatory reduction of NO 3 2 and SO 4 22 as sources for organic nitrogen and sulfur. During the degradation of mineral- poor organic substances (wood, straw) bacteria must assimilate inorganic nitrogen and phosphorus, thus e?ectivelycompeting withplants forthese nutrients. Nitrogen ?xation is an assimilatory process that occurs exclusivelyinsomebacteria.Itisananaerobicprocessand the ability to ?x nitrogen is especially common among anaerobesandmicroaerophiles;italsooccursamongsome aerobes (many cyanobacteria, Azotobacter, Rhizobium) that have special adaptations to protect the nitrogenase complex fromoxygenexposure. Roles of Bacteria in Nature Thefundamentalanduniquerolesofbacteriainnatureare (1) as links in food chains between detritus (including Table 1 Principaltypes of bacterial energy metabolism Fermentation: Anaerobic processes involving the dismutationof (organic)molecules; no externalelectron acceptor. Low energy yields. Metabolites includevariouslow molecularweight organic compounds(alcohols, fatty acids) and hydrogen. Complete fermentation toacetate plus hydrogenrequires alow ambient hydrogen tension. Respiration: Aerobicrespiration: oxidationofsubstrateswithoxygen.Organotrophsoxidizeorganicmatter;principalmetabolitescarbon dioxideand water. Carriedout by alargenumberof aerobicbacteria that di?er (among otherproperties) with respect to which polymers they can hydrolyse. Specialized aerobes, the chemolithotrophs, oxidize inorganic substrates. Nitri?ers oxidizeNH 4 1 toNO 3 2 (viaNO 2 2 );colourlesssulfurbacteriaoxidizeH 2 StoS o andSO 4 22 ,andmethanotrophsoxidizeCH 4 . Many bacteriacatalyse theoxidation ofreducedironandmanganese; energyconservationfromthisprocesshasnot been demonstrated inall cases. Anaerobicrespiration: useofexternalelectronacceptorsotherthanoxygen.Inmostcasestheinvolvedspeciescanuseonlya limited number oflow molecularorganic compounds inaddition tohydrogen. They thus depend on metabolites of fermentingbacteria.Denitri?ersuseNO 3 2 andproduceN 2 (andsomeotherNcompounds)asmetabolites.Sulfatereducers useSO 4 22 andproduceH 2 S.ManganeseandironreducersuseMn 41 andFe 31 toproduceMn 21 andFe 21 ,respectively. Methanogenesis: Methanogens produce CH 4 from CO 2 1H 2 or by dismutation of acetate into CO 2 1CH 4 . Some methanogens canalso use reduced C1 compounds (e.g. methanol) toproduce CH 4 . Phototrophy: Oxygenicphotosynthesis occursincyanobacteria.Lightenergyisharvestedtoreducecarbondioxidetoorganicmatter,using water asreductant and producing oxygen asa metabolite. Anoxygenic photosynthesis implies the use ofreductants other than water (primarily H 2 S,H 2 and Fe 21 ). Occurs among several bacterial groups such asin, for example, purple and green sulfur bacteria. Bacterial Ecology 4 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net dissolvedorganicmatter)andbacterivorousprotozoaand animals, (2) their dominance as mineralizers of organic carbon,and(3)catalysisofessentialchemicalprocessesin thebiosphere.Intheextantbiospherethemostimportant primary producers are constituted by vascular plants (on land)andbyalgae(inthesea).Photosynthesisresultsina 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 miner- alization processes are complex and they drive the major biogeochemicalcycles ofcarbon,nitrogen,andsulfur. Bacteria as primary producers In certain environments, especially in nutrient-depleted oceanic waters, unicellular cyanobacteria play a substan- tial role as primary producers as compared to eukaryotic algae. Colonial ?lamentous cyanobacteria may tempora- rily play a similarly important role in shallow seas and in lakes; the capability of nitrogen ?xation renders cyano- bacteria superior competitors among phototrophs when waters become depleted in reactive nitrogen, but when phosphateisstill available. Other types of bacterial autotrophs are, of course, also primaryproducersinthesensethattheyassimilatecarbon 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 sul?de) originally derives from plant tissue that has been degraded under anaerobic conditions. In a biosphere context, these organisms then rather exemplify thecomplexitiesofmineralizationprocesses.Chemoauto- trophic bacteria associated with hydrothermal vents depend on substrates (sul?de, methane) deriving from geothermalprocesses;again,however,theseresourcescan onlybeexploitedinthepresenceofoxygenthatoriginally derives from photosynthesis. Bacteria as links in food chains Alargepartoftheprimaryproduction(inmanyecological 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 forlargeranimals(Figure 5).Theconcepthasbeenreferred 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 incapableofhydrolysingmostpolymericplantcompounds andmostplanttissueisverypoorinessentialnutrients,e.g. nitrogenandphosphorus.Finally,animalsarenotcapable of utilizing dilute solutions of organics, nor the (energy- containing)endproductsofanaerobicdegradationsuchas methaneorhydrogensul?de. Conversely, bacteria are capable of degrading all naturally occurring polymers and they can assimilate dissolvedinorganicnutrientsfromtheenvironment.They are extremely e?cient in assimilating dissolved organic material, converting it into particulate food that is available to phagotrophs. Also, specialized chemolitho- trophic bacteria can harvest the energy of, for example, dissolved sul?de to produce bacterial cells. Bacteria thus playanessentialroleasfoodchainlinksbetweenprimary productionandanimals. Biogeochemical cycling Bacteria constitute the most important agent for the mineralization of organic carbon in almost all natural ecosystems.Inthiscontextanumberofessentialprocesses inthebiosphereareexclusivelycatalysedbybacteria.One such example is the generation of methane (by methano- genic bacteria in certain anaerobic habitats; some atmo- spheric methane, however, also derives from geothermal processes in the Earth?s crust) and the re-oxidation of methanebyothertypesofbacteriainaerobicenvironments such as soils (some methane oxidation also takes place through photochemical processes in the upper part of the atmosphere).Bacteriaalsotransformandcontrolconcen- trations of a number of other atmospheric trace gases (Conrad, 1996). The global nitrogen cycle provides an example of the importanceofbacterialprocesses.Atmosphericnitrogenis made available to the biota through bacterial nitrogen- ?xation (some nitrogen is oxidized in the atmosphere duringelectricdischarges;theresultingnitrogenoxidesare 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 Primary producers Bacteria Dissolved organic compounds Particulate detritus Food chain 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. Bacterial Ecology 5ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net ammonia to nitrate is a bacterial process. So is dissim- ilatorydenitri?cation;itsprincipalproductisnitrogen,and this represents the only mechanismby which atmospheric nitrogen isreplenished. Bacteria play a substantial and often unique role for a number of other biogeochemical processes, including the oxidationandre-oxidationofmetals,dissimilatorysulfate reductionandsul?deoxidation,andcarbonatedeposition anddissolution. Bacterial Symbioses Manyexamplesofsymbioticbacteriawithinoronanimals, plants and protists have been described. Among them many are poorly understood while others have been studied extensively due to their great economic signi?- cance. The following refers mainly to such well-studied cases. Symbiotic nitrogen fixation While free-living nitrogen-?xing bacteria occur it is believedthatbyfarthelargestshareofterrestrialnitrogen ?xationtakesplaceinsymbioticrelationswithplants.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 speci?c 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.Thebacteriainvaderootcellsandformnodules;they thentransformintoswollenbacterioids.Thebacterioids?x nitrogenandfeedthehostplantwithnitrogenintheform ofammonia;inreturnthehostprovidescarbonsubstrates for the bacteria. A special feature is the presence of a haemoglobin(whichisjointlysynthesizedbythebacterium 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 sweetgale)harbourthenitrogen-?xingbacteriumFrankia in root nodules. Other plants harbour cyanobacterial symbionts(cycads,thewaterfernAzolla);thesesymbioses also are importantfortheirnitrogen ?xation. Symbiotic polymer degradation Many herbivores, especially mammals belonging to di?erent taxa, have solved the problem of low nitrogen andphosphoruscontentsintheirfoodandtheinabilityto utilize structural plant polymers by hosting a consortium of anaerobic bacteria that ferment polysaccharides into lowmolecularfattyacids;thesearethenassimilatedbythe animal. Ruminants(andkangaroos andafew other types ofherbivorousmammals)havepregastricfermentation.In cows and sheep, the rumen is anatomically a part of the oesophagusanditconstitutes10?15%ofthevolumeofthe animal.Therumenisafermentationchambercontaininga 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 thetruestomachandconstitutethesoleproteinsourcefor the host animal. Excreted urea is recycled via saliva as a nitrogen source for the microbial biota. Adult ruminants areentirelydependentontheirmicrobialsymbionts.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 amongnonmammaliananimals;ithasbeenreportedfrom a few species of birds, reptiles and ?sh. Among inverte- brates it has been found in certain sea urchins and shipworms;termiteshavesymbioticcellulosedegradation, but in most termite groups the principal cellulose decom- posersare eukaryoticmicroorganisms. Other examples of bacterial symbioses Many other kinds of bacterial symbioses exist; these are generally of no or little economic signi?cance and appear more exotic. Many marine benthic invertebrates harbour symbiotic chemolithotrophic bacteria. These are mainly colourless sulfur bacteria although two cases of methane- oxidizingsymbiontshavealsobeenfound.Suchsymbioses haverecentlybeenfoundtooccurwithinseveralgroupsof 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 sul?de through di?erent 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 bacterialsymbiontsastoolsof?biologicalwarfare?suchas Bacterial Ecology 6 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net thesymbiontsofcertainstrainsoftheciliateParamecium: whenthebacteriaarereleasedinthewatertheykillother, 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 speci?c and essential to their hosts have been described, but their true adaptive signi?canceremains tobe discovered. References Conrad R (1996) Soil microorganisms as controllers of atmospheric tracegases(H 2 ,CO 2 ,CH 4 ,OCS,N 2 O,NO).MicrobiologicalReviews 60: 609?640. Ghiorse WC (1997) Subterranean life. Science 275: 789?791. Southward EC (1987) Contribution of symbiotic chemoautotrophs to thenutritionofbenthicinvertebrates.In:SleighMA(ed.)Microbesin theSea, pp.83?118. New York: Wiley. Further Reading Armitage JP and Lackie JM (eds) (1990) Biology of the Chemotactic Response. Cambridge: CambridgeUniversity Press. Balows A, Tru¨ per HG, Harder W and Scheifer K-H (eds) (1991) The Prokaryotes, vols 1?4,2nd 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 Biogeochem- istry.TheEcophysiologyofMineralCycling,2ndedn.SanDiego,CA: Academic Press. FenchelTandFinlayBJ(1995)EcologyandEvolutioninAnoxicWorlds. Oxford: Oxford University Press. FletcherM,GrayTRGandJonesJG(eds)(1987)EcologyofMicrobial 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) Di?usion. The crucial process in many aspects of the biologyof bacteria. Advances inMicrobial Ecology 11: 37?70. 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 Micro- organisms, 8thedn. UpperSaddle River, NJ: Prentice Hall. Postgate J (1982) The Fundamentals of Nitrogen Fixation. Cambridge: CambridgeUniversity Press. Smith DC and Douglas AE (1987) The Biology of Symbiosis. London: EdwardArnold. Tate RL(1995) SoilMicrobiology. New York:Wiley. Bacterial Ecology 7ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net A0339 1..7