principles of microbial ecology

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Microbial Ecology: Searching for PrinciplesThe extraordinary diversity of microbial ecosystems complicates effortsto develop principles encompassing microbial ecology

Allan Konopka

Modern microbial ecology spansapproximately 50 years. Al-though Martinus Beijerinck andSergei Winogradsky both thoughtabout ecological niches in the

early part of the 20th century, they approachedthe challenge by trying to cultivate microbesunder simulated natural conditions. Hence, Iconsider Robert Hungate the first truly modernmicrobial ecologist. Focusing on rumen mi-crobes, he and his colleagues dealt directly withthe ecosystem of these microorganisms. Insteadof limiting their efforts to isolating and identify-ing microorganisms of the rumen, Hungate andhis collaborators also measured their activitiesin situ. In 1966, Hungate publishedThe Rumenand its Microbes, synthesizing years of research

to better understand that ecosystem.Microbial ecology has grown substantially

since then. For instance, more than 2,200 mem-

bers of ASM consider the microbial ecologydivision their primary or secondary affiliation.Interest on the international scale is also strik-ing. This growth in interest continues to spur agreat deal of research, expanding our breadth ofdetailed knowledge about many different micro-bial ecosystems. However, this growth in inter-est has not led to a synthesis of the field as awhole. The last overarching view of microbialecology was published 40 years ago by ThomasBrock in the influential book, Principles of Mi-crobial Ecology. Thus, it is time to reexaminethe key principles of microbial ecology.

Analytic Tools Expand Knowledge,Necessitating a Review of Principles

As in other fields of science, new technologiesstimulate ecology research, and ecologists haveproved adept at adopting analytic toolsfrom other

fields. For instance, radioisotopes came intouse during the early 1950s foruse in determin-ing in situ flux rates in a wide variety ofecosystems. Microbial ecologists during the1980s learned through microelectrode-basedanalyses that microbes deal with gradients onvery small distance scales. Meanwhile begin-ning in the mid-1980s, Norman Pace and hismany collaborators began applying molecular

biology techniques to study microbial ecosys-tems. Those efforts continue to build momen-tum, providing a wealth of insights into thedistribution and natural history of microbes.

These and other powerful analytic tech-niques are being applied to the extraordi-nary diversity of habitats occupied by mi-crobes. Faced with the wealth of specificinformation gained from these studies, thereare solid reasons for reviewing the princi-ples underlying microbial ecology.

Summary

Amid recent growth in knowledge about micro-bial ecology, it is time to reexamine key princi-ples and to identify new ones.

Identifying the principles of microbial ecologywill benefit students entering this field, andcould lead to better cooperation with ecologists

working in related fields.

To understand the interactions of a microbewith its environment, one should consider theimmediate microenvironment before assessingits wider dynamic effects.

Developing an ecotype concept would benefitmicrobial systematics and microbial ecology,and will depend on cooperation among physiol-ogists, ecologists, and bioinformaticists.

Persp

ective

Volume 1, Number 4, 2006 / Microbe Y 175

Allan Konopka is

Professor of Biolog-

ical Sciences in the

Department of Bio-

logical Sciences,

Purdue University,

West Lafayette, Ind.

akonopka@purdue

.edu


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For one thing, such a review will provide abetter framework for young scientists when theybegin to evaluate the idiosyncrasies of particularsystems that they may be studying. This effort

will benefit not only those who are consideredcard-carrying microbial ecologists, but also sci-entists in allied fields. Communicating the prin-ciples of microbial ecology to colleagues whostudy macrobiota also could have an impact ongeneral ecological theory, and could help tobetter identify areas where microbial ecologyshould develop independently.

Further, a statement of principles provides aframework for evaluating what may be novel inan exceptional system and can lead to a deeperunderstanding of a field. In the case of microbial

ecology, developing a statement of principles isperhaps more difficult than in other areas ofmicrobiology because of the extraordinary di-versity of microbial ecosystems. In other fields, acritical mass of scientists focuses on a modelsystem. The synergy among them can lead torapid developments and the evolution of funda-mental principles. For example, many funda-mental principles of molecular genetics andtranscriptional regulation arose from an intensefocus on studyingEscherichia coli.

Because microbial ecology research programsare being supported by several funding agencieswith different missions, that sharp focus on asingle entity is not likely to be repeated. Hence,microbial ecologists willneed to consider howbestto synthesize phenomena and to search for funda-mental principles among disparate ecosystems.

Defining the Boundariesof Microbial Ecology

The 19th-century German biologist Ernst Hae-ckel coined the termoekologie, based in part on

the Greek word for house, to describe thestudy of organisms in the context of theirhouseholds in nature. Because microbialecologists study interactions of microbeswith their abiotic and biotic environments,

their focus differs somewhat from those whostudy environmental microbiology or puremicrobial diversity. Although the study ofmicrobial diversity has important implica-tions for evolution, systematics, biotechnol-ogy, and ecology, it is distinct from micro-bial ecology. Ecological studies examine notonly the natural history of a microbe, includ-ing its distribution and abundance in relation-

ship to its environment, but also investigate themechanisms underlying its distribution.

One very important implication of Haeckelsdefinition is that the authentic ecology of mi-crobes occurs on spatial scales of nanometers tomicrometers. Nonetheless, microbial activitiescan affect the environment on a much largerscale because ecological systems operate on somany different scales. Microbial ecology can beviewed as a study of these different (yet inter-connected) systems (see box, above). In the lastdecade, the term systems biology has beenapplied to the study of complex processes at theorganism level; however, those studying ecologyanalyze complex systems that similarly embodyemergent properties.

Living and abiotic processes affect one an-other at the global and landscape scales. Forexample, arid conditions in the African desertcan stimulate iron-limited photosynthesis wheniron-containing dust particles are transportedover thousands of kilometers to distant oceanicsites. At the ecosystem level, there are complexand complementary interactions among physi-cal, chemical, and biological components.

However, to understand the interactions of amicrobe with its environment, one should firstconsider the immediate microenvironment (Fig.

1). By focusing on this scale, we can describe theimportant physical and chemical characteristicsof a minimum set of microbial ecosystems (seetable). However, it is apparent that some char-acteristics overlap. For example, a planktonicmicrobe in the metalimnion, or mid-layer, of athermally stratified lake may exploit verticalgradients of nutrientshowever, the gradientshave a spatial scale of meters rather than themillimeters typical of a microbial mat. Impor-tantly, one should not lose sight of the dynamic

Spatial Scales of Microbial Ecology

Global and landscape scaleAquatic and terrestrial biomes

Macroscopic scalePhysical/chemical/biological interactionswithin ecosystems.

Aquatic systems: planktonic vs. benthic habitatsTerrestrial systems: saturated vs. unsaturated soilsMacroorganism-associated ecosystems: tissue-specific habitats

Microscopic scaleSystem dynamics near and within a microbialcell

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impact of microbial activity, even if it appears tobe confined to a microscopic system. Those dy-namics often produce effects at the macroscopicand landscape levels.

Overarching Principles for MicrobialEcology

One means for uncovering the principles of micro-bial ecology entails envisioning how microorgan-isms interact with their environmentsat the micro-scopic scale. The principles then can be dividedinto three groupsoverarching themes, popu-lation ecology, and physiological ecology.

Microbes comprise nearly half of all biomasson earth. All habitats suitable for plants andanimals also harbor microbial populations. Inaddition, some microbes are adapted to grow un-der physical and chemical conditions that are tooextreme for plant and animal growth.

The primary role of microbes in the biosphereis as catalysts of biogeochemical cycles. That is,microbes mediate kinetically inhibited but ther-modynamically favorable reactions. Some mi-crobes may also have strong effects on the ecol-ogy of specific micro- or macro-organisms, viatheir roles as pathogens or symbionts.

The effects of microbial catalysis on the rates ofchemical and energy flow through an ecosystem

depend upon the population size of microbesthe number of catalystsand the physiologicalactivity of those microbes (as determined byextant physical and chemical conditions).Instable ecosystems, small numbers of mi-crobes can still produce significant effectsover geological time spans.

The results of microbial catalysis can haveprofound effects on the physical and chemi-cal characteristics of the macroenvironment.However, microbial activity is determinedby the physical and chemical characteristics

of the microenvironment, which is measuredon a micrometer scale.Microbes exhibit greater metabolic versa-

tility than do macroorganisms.This versatil-ity is expressed in at least four differentways. Microbes can use essentially all re-duced chemicals on earth as an energy sourceprovided that the oxidation of a specific chem-ical can be coupled to reduction of a terminalelectron acceptor in a thermodynamicallyfavorable reaction. Some microorganisms

metabolize broad ranges of substrates. Complexmicrobial communities contain metabolically dif-ferent populations, whose diversity provides resil-ience in the face of environmental perturbations,

reducing the chance that extreme conditions willkill all the species performing a particular eco-logical function. Microbial populations are ca-

Microbial-scale ecosystems

Ecosystem type Examples Characteristics

Planktonic Open ocean, lakes Oligotroph lifestyle; high-affinity uptake of multiplenutrients

Surface associated(saturated water)

Freshwater and oceansediments,subsurfacesediments, microbialmats, biofilms

Gradient lifestyle;hydrodynamic processes andfluid flow determine nutrientfluxes; biomass densityaffects gradient steepness

Surface associated(unsaturated water)

Surface and vadosezone soils

Water availability limitsactivity and dispersal;dormancy; patchy nutrientdistribution

Macroorganism associated Gastrointestinal tract,rhizosphere, epiphytes

Co-evolution; specificmolecular interactions withsurface associated molecules

F I G U R E 1

Processes at the microenvironment scale.



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pable of rapid evolutionary responses to envi-ronmental perturbations as a result ofmechanisms that generate relatively high muta-tion frequencies as well as horizontal gene trans-fers across large phylogenetic boundaries.

Population Ecology

The types and numbers of different microbespresent in a habitat are a function of the diver-sity and amounts of nutrient resources available,modulated by the organisms ability to withstandforces that eliminate it from the habitat. Lossforces may be biotic, involving predators or para-sites; physical, such as flushing or scouring actions;or physiological, such as a lack of nutrients.

Microbial populations may exhibit larger dy-namics in biomass, composition, and activity

than do plant and animal populations. Thesecomplex, nonequilibrium dynamics are conse-quences of several factors, including the tempo-ral frequency of changes in important environ-mental factors, the rapid pace of physiologicaladaptation by microbes to changing environ-mental conditions, positive and negative inter-actions between different microbes, and the ca-pacity for rapid genetic change.

An important consequence of these popula-tion-based principles is that neither environ-mental nor biological factors by themselves de-

termine the observed temporal changes inmicrobial populations. Instead, those changestypically depend on intricate interactions amongthese factors.

Physiological Ecology

Shortages of a single essential resource are suf-ficient to limit the microbial biomass that accu-mulates in a particular ecosystem. This principlerestates the law of the minimum, which Ger-man scientist Justus von Liebig formulated dur-ing the 19th century. Any nutrient resource that

microbes take up may be conserved as part of thebiomass, used as an energy source and terminalelectron acceptor, or can function as both a com-ponent of biomass and a source for energy.

In the ecology of macroorganisms, the case inwhich nutrient resources determine the level ofbiomass is termed bottom-up control. Nutri-ent resources are not limiting in top-down con-trolled systems because a predator or parasitemaintains the biomass level below the carryingcapacity of the system.

Growth of microbes on the limiting nutrient(or a set of nutrients) will depress its concentra-tion to a value that limits microbial growth rate.The real limitation is upon the rate of nutrienttransport into the cytoplasm. Hydrodynamics

or mass transport may limit the nutrient fluxrate in an ecosystem.Competition among microbes for low con-

centrations of a limiting nutrient and temporalvariability in its availability both serve as strongselective forces in natural habitats. Physiologicaland morphological characteristics can haveadaptive value under specific conditions. Thosevariants may include the number, diversity, andaffinity of transporters in cell membranes; regu-lation of the capacity to take up nutrients; cellsize, due to the change in surface area to volumethat impacts capacities for substrate uptake ver-sus assimilation; types of storage polymers; met-abolic versatility; motility and chemotaxis; andcapacity to survive during nutrient shortages.

The cell surface interacts critically with the ex-ternal environment. This interaction affects nutri-ent uptake and metabolite excretion, signaling be-tween cells, and both specific or nonspecificinteractions with biotic and abiotic surfaces.

The Relationship of MacroorganismalEcology to Microbial Ecology

Many principles that were developed with theecology of plants and animals in mind also applyto microbes. Microbial ecosystems can provideadvantages for researchers who are testing eco-logical theories that would be difficult to addressthrough experiments involving plants or ani-mals. Both microbial and macro-scale ecologistshave recognized that professional interactionshave not been as effective as possible; therefore,renewed efforts to develop mutual awarenesswould benefit both areas of ecology.

However, in at least two areas, the principles

of macroorganism ecology do not readily applyto microbial ecology. One such area is commu-nity ecology, in which the analysis of interac-tions of organisms at different trophic levels viafood-web analysis is an important component.With the exception of the microbial loop inaquatic ecosystems, microbial ecologists havenot focused on trophic-level interactions. How-ever, microbial ecologists are becoming increas-ingly aware of the impact of viruses as predatorson microbes.

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The other area, which focuses on the effects ofthe environment on evolutionary developmentalbiology, is still a relatively new one for ecolo-gists who study plants and animalsin part,accounting for why it is not yet a subject for

microbial ecologists. However, because somepopulations of microbessuch as those in bio-filmsare multicellular, they could be exam-ined from this perspective.

Missing Principles, Implications for the

Future of Microbial Ecology

Some areas of research in microbial ecology donot lend themselves to the framing of generalprinciples either because there is no consensusregarding experimental observations or because

no fundamental concept has emerged. In partic-ular, it is problematic to formulate conceptsregarding species diversity and the effects oftime, space, and environmental heterogeneitiesupon diversity patterns.

These difficulties reflect a continuing ambiva-lence as to what constitutes a bacterial species.In an ecological context, this ambivalence re-volves around the difficulty in defining anecotypea genetically cohesive populationwhose functional ecology is distinct from others.Analysis of genome sequences illuminates the

nature of the problemsequences of multiplestrains from one bacterial species may differ sub-stantially from one another. Strains appear to gainor lose genetic modules, and those changes cansubstantially alter their respective physiological

properties. How then does a microbial ecologistassess functional diversity in a habitat?

During the 1970s and 1980s, microbial ecol-ogists made significant progress in determiningrates of microbial activities in natural habitats.

Despite that progress, they found it difficult todetermine which particular microorganismswere most important in catalyzing reactionswithin those habitats. Over the past 15 years,however, microbial ecologists have made enor-mous progress determining the breadth of mi-crobial diversity in nature, albeit without simul-taneously analyzing physiological processes.

These two separate lines of inquiry need tofuse, and there are new experimental strategiesfor doing so. For instance, physiological andnucleic acid-based techniques can be combinedto identify the microbes in natural habitats thatcatalyze biogeochemical processes.

The most pressing concerns come from thoseareas where principles are missing because welack fundamental concepts. For instance, wecannot understand functional diversity withoutfirst agreeing on what biological units to study.Ecological insights might be combined withmultilocus nucleotide sequence analyses to pro-vide a path towards defining ecotypes.

Developing an ecotype concept would benefitmicrobial systematics and microbial ecology,and will depend on a partnership developing

between physiological ecologists and bioinfor-maticists. Genome sequences arrive at a breath-taking rate. Can our understanding of the phys-iological responses of microbes to theirenvironments keep pace?

ACKNOWLEDGMENTS

I thank Jim Fredrickson, Mike Madigan, Brian Oakley, Jim Staley, and Dave Ward for their comments and discussion.

SUGGESTED READING

Andrews, J. H. 1991. Comparative ecology of microorganisms and macroorganisms. Springer, New York.Andrews, J. H. 1998. Bacteria as modular organisms. Annu. Rev. Microbiol. 52:105126.

Brock, T. D.1966. Principles of microbial ecology. Prentice-Hall, Englewood Cliffs, N.J.Gevers, D., F. M. Cohan, J. G. Lawrence, B. G. Spratt, T. Coenye, E. J. Feil, E. Stackebrandt, Y. Van de Peer, P. Vandamme,F. L. Thompson, and J. Swings. 2005. Re-evaluating prokaryotic species. Nature Rev. Microbiol. 3:733739.Madsen, E. L. 2005. Identifying microorganisms responsible for ecologically significant biogeochemical processes. NatureRev. Microbiol.3:439446.Olsen, G. J., D. J. Lane, S. J. Giovannoni, N. R. Pace, and D. A. Stahl. 1986. Microbial ecology and evolution: a ribosomalRNA approach. Annu. Rev. Microbiol.40:337365.Rossello-Mora, R., and R. Amann.2001. The species concept for prokaryotes. FEMS Microbiol. Rev. 25:3967.Weinbauer, M. G.2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev.28:127181.Whitman, W. B., D. C. Coleman, and W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA95:65786583.


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