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PERSPECTIVES
ESSAY many areas in which microorganisms are of
environmental and economic importance.
For example, improved quantitative theory
The role of ecological theory could increase the efficiency of wastewater
treatment processes, through the predic-
in microbial ecology tion of optimal operating conditions and
conditions that are likely to result in system
failure. Quantitative information on the
James I. Prosser, Brendan J. M. Bohannan, Tom P. Curtis, Richard J. Ellis, links between microbial community structure,
Mary K. Firestone, Rob P. Freckleton, Jessica L. Green, Laura E. Green, population dynamics and activities will also
Ken Killham, Jack J. Lennon, A. Mark Osborn, Martin Solan, facilitate assessment and, potentially, mitiga-
Christopher J. van der Gast and J. Peter W. Young tion of microbial contributions to climate
change, and should lead to quantitative
Abstract | Microbial ecology is currently undergoing a revolution, with predictions of the impact of climate change
repercussions spreading throughout microbiology, ecology and ecosystem science. on microbial contributions to specific eco-
The rapid accumulation of molecular data is uncovering vast diversity, abundant system processes. Given the high abundance,
uncultivated microbial groups and novel microbial functions. This accumulation of biomass, diversity and global activities of
data requires the application of theory to provide organization, structure, microorganisms, the ecological theory that
has been developed for plants and animals
mechanistic insight and, ultimately, predictive power that is of practical value, but is of limited value if it does not apply to
the application of theory in microbial ecology is currently very limited. Here we microbial communities. Microorganisms
argue that the full potential of the ongoing revolution will not be realized if arguably provide much better controlled and
research is not directed and driven by theory, and that the generality of established more manipulable experimental systems
ecological theory must be tested using microbial systems. for testing ecological theory than plants
or animals, and such testing is essential to
establish the generality of theory. The use of
Bacteria and Archaea have an essential microbial processes (in, for example, better controlled microbial systems might
role in earth system processes. They are wastewater treatment, industrial chemical also generate new theory that is relevant to
ubiquitous, possess enormous metabolic and production, pharmaceutical production and plants and animals.
physiological versatility and are essential to bioremediation), and the realization that Two factors limit the development of
virtually all biogeochemical cycling proc- many nonspecific microbial processes such theory in microbial ecology. The first
esses — microbial carbon and nitrogen are as biogeochemical cycling are essential for is a lack of data and associated insights.
calculated to be, respectively, equivalent to ecosystem sustainability, understanding the This is due in large part to the difficulties
and tenfold as great as the carbon and nitro- factors that control these processes is crucial. inherent in observing microorganisms in
1 –6
gen stored in plants . Although small (~10 In our view, this can best be achieved by nature, which often have few distinguishing
30
m), they are abundant (>10 individuals generating theory that is based on existing morphological features and often cannot
globally). Their phylogenetic and physiologi- observations and subsequent experimental be cultivated in the laboratory. The applica-
cal diversity is considerably greater than that validation. tion of cultivation-independent molecular
of animals and plants and their interactions techniques and their successors — genom-
with other life forms are correspondingly The importance of theory ics, metagenomics, transcriptomics and
more complex. Theory is used to classify, interpret and proteomics — has generated a plethora of
Understanding the ecology of micro- predict the world around us. Without it, new and more comprehensive observations
organisms is arguably one of the most microbial ecology is merely the accumula- of microorganisms in nature, but we still
compelling intellectual challenges facing tion of situation-bound statements that lack the theoretical tools required to detect
contemporary ecology. Although worthy for are of limited predictive ability, providing underlying principles and mechanisms.
its intellectual merits alone, developing such microbiologists with few insights. Theory The second factor is cultural, in that the
an understanding is essential to meet many has an essential role in developing an under- tools and disciplines of ecological theory
of the major challenges facing human society standing of, and explaining the interactions are not part of the contemporary mindset
today, such as the management of natural between, microorganisms and their physical, in microbiology. Ecological theory and
ecosystems and the mitigation of climate chemical and biological environments. quantitative reasoning typically form only
change. Despite this, the application of theory This understanding will be lacking if it is minor components of education in microbi-
is severely lacking in microbial ecology solely qualitative, and a full understanding ology, and microbiologists have traditionally
where, paradoxically, it is required most. Just therefore requires quantitative theory. used a detailed, reductionist approach that
as ecological theory arose from natural his- Theory generates predictions that can be is based on understanding physiological
tory to draw generalized conclusions from of practical value for policy makers, stake- mechanisms, with relatively little attention
specific observations of organisms in their holders and society. A striking example is the paid to theory. Although the challenge
environment, so microbiologists need theory use of epidemiological models to predict for the microbial ecologist might appear
to interpret the plethora of observations the spread of human and plant pathogens to be the discovery (or recollection) of ever-
that have been made since van Leeuwenhoek and the use of these predictions to inform and more fascinating details of a given system,
2
first saw animalcules more than 300 years implement control policies . There is similar the theoretician aims to predict as much as
ago. With the increasing reliance on specific potential value in applying theory in the possible about a system using as few of these
384 | MAY 2007 | VOLUME 5 © 2007 Nature Publishing Group www.nature.com/reviews/micro
PERSPECTIVES
details as possible; but the populations and systems and allow the much more effective might not lead to simple mapping between
structures of microbial communities, by management of the natural world. molecular markers and an ecological niche.
comparison with those of plants and ani- In the following sections we discuss More crucially, speciation, and ecological
mals, remain inscrutable. The application of examples of areas of ecological theory that species definitions, must consider bacterial
molecular techniques has demonstrated the might be particularly valuable in microbial gene-transfer processes, which are erratic
need for discovery research, but in our view ecology. In doing this, we attempt to deter- and transfer only a small part of the genome.
this can only be exploited if it is directed mine whether the particular characteristics They provide a potential mechanism for
by insights gained from the application of of microorganisms present difficulties in maintaining biological species in Mayrs
8
theory. applying ecological theory that has been sense , because an incoming gene can
developed for plants and higher animals. replace the homologous copy in the genome,
Current ecological theory We consider whether and where new theory maintaining the genetic cohesion of the
An established body of theory exists for might be required for microorganisms to species. In addition, these processes can also
plant and animal ecology but the differ- enhance or replace established ecological result in the horizontal transfer of genes with
ences between microorganisms and large theory. We also identify conceptual and no counterpart in the recipient that can be
organisms, and the extent to which these dif- practical challenges faced by microbial maintained on a plasmid or integrated by
ferences restrict the applicability of existing ecologists in applying quantitative ecological non-homologous recombination. However,
theory to microbial ecology, often form an theory. the importance of homologous recombina-
impasse that is tacitly accepted and seldom tion and horizontal transfer varies widely
questioned. Commonly cited differences Ecological species concepts among well-studied bacterial species, and
include the small size of microorganisms, Most ecological theory depends on a con- perhaps even more so among the uncultured
high rates of population growth, high rates cept of species: population ecology counts masses in the environment. This hetero-
and extent of dispersal, the vast abundance individuals within species whereas com- geneity is one reason why we are still far
of microorganisms, and the unique aspects of munity ecology and macroecology count from a consensus on the nature of bacterial
their biology (such as parasexuality or the number of species. Species are most species, as revealed at a recent Royal Society
discussion meeting9
extremely hardy resting stages). However, commonly defined through the biological .
the breadth of distribution of many of these species concept promoted by Mayr4. This is A consequence of gene transfer is that
traits among microorganisms in nature is a genetic definition that envisages a species the bacterial genome is thought to consist
not known. Furthermore, the existence of as a group of interbreeding individuals that of two distinct parts, the core genome and
10
these traits does not necessarily prevent the is isolated from other such groups by bar- the accessory genome . The core genome
application of existing ecological theory riers to recombination. If genetic exchange comprises genes that are essential in most
to microorganisms (see later discussion of within a species is sufficiently extensive, circumstances and might form the basis for
seed banks). Also, the relatively and that between species is sufficiently low, Mayrian species that maintain coherence
spores and
large scales of time and space over which species will be relatively homogeneous in through homologous recombination. The
most microorganisms are studied does themselves and ecologically distinct from accessory genome encodes special ecological
not necessarily preclude the application of other species. Unfortunately, prokaryotes adaptations in genes that are readily gained
existing theory; theory related to the subdis- (and some eukaryotes) are asexual, thereby and lost. Strains that belong to the same
cipline of ecology called macroecology was violating these assumptions, and do not species, as defined by their core genome, can
developed specifically to further the under- form species in this genetic way. An differ in the presence and absence of hun-
standing of ecology on large scales of space alternative, the ecological species concept, dreds of accessory genes, and consequently
and time (see below). The challenge facing defines a species as a set of individuals can have different ecological capabilities.
microbial ecologists, and indeed all ecolo- that can be considered to be identical in all According to this view, Cohans ecotypes are
gists, is to match the appropriate theoretical 5 has merely temporary lineages with particular
relevant ecological properties. Cohan
approach to the organism, system, scale and argued that bacteria have ecological species constellations of accessory genes, and the
question of interest. (ecotypes). He postulates that bacteria ecological niche cannot explain the apparent
Microbial model systems have played an occupy discrete niches and that periodic cohesion of species that are defined by the
important, although often underappreci- selection will purge genetic variation 11.
phylogeny of core genes
ated, part in the development of existing within each niche without preventing Surveys of 16S ribosomal RNA (rRNA)
ecological theory (reviewed in REF. 3), divergence between the inhabitants of dif- gene sequences have demonstrated the huge
demonstrating its general applicability to ferent niches. So, genetically and ecologi- diversity of bacterial communities, but if
microorganisms. However, it is less common cally distinct species will arise, provided much of the interesting ecological adapta-
for existing theory to be applied to micro- there is little or no recombination, and tion is conferred by the accessory genome
organisms in nature despite the fact that this ecological theories that assume such spe- then the true ecological diversity exists in the
would be valuable. It would be extraordinar- cies should apply to bacteria. This also rich brew of catabolic plasmids, resistance
ily inefficient to attempt to reinvent existing predicts that molecular diversity should transposons and pathogenesis islands. These
theory for application to microorganisms. relate directly to ecological diversity. can be shared among disparate bacteria in an
Furthermore, the application of existing Cohans ecotypes depend on discrete environment that favours them, but can be
theory would afford ecologists the opportu- niches but speciation is more difficult to absent in the same bacterial species growing
nity to test the true generality of ecological envisage when the relevant environmental elsewhere. The methods of evolutionary
principles and to create a synthetic ecology variables are continuous. Bacterial speciation ecology have been applied to the interaction
that spans all organisms. This would greatly in these situations could be explored using between these accessory elements and their
increase our understanding of ecological the theory of adaptive dynamics6,7, but this host bacteria. For example, Bergstrom and
NATURE REVIEWS | MICROBIOLOGY © 2007 Nature Publishing Group VOLUME 5 | MAY 2007 | 385
PERSPECTIVES
17
Box 1 | Theoretical approaches for estimating diversity in a sample hybridization (BOX 1). Gans and colleagues
highlight the requirement for collectors
A species abundance curve is simply a graph in a Species curve curves of in excess of one million PCR-
which the abundance of a particular species is Area under species curve = S derived clones to ensure coverage of 80% of
t
plotted on the x axis and the number of species at bacterial species within a 1-g soil sample.
that abundance is plotted on the y axis (see Without screening large numbers of clones,
figure). The observation and contemplation of 1/a sampling low-abundance species remains a
these distributions is supported by a rich literature matter of chance.
in conventional ecology in which some research, 16S rRNA gene sequences provide an
but not all, has imbued such distributions with Log (N ) Log (N ) Log (N )
some ecological meaning. However, microbial 2 min 2 0 2 max operational measure of species. High-
18
ecologists have an interest in species abundance Number of species S throughput sequencing or SARST (serial
19
curves because the area underneath a species analysis of ribosomal sequence tags) are
abundance curve is the total diversity. This currently the best suited techniques for
presents us with a ‘catch 22’ situation: we cannot 0 5 10 15 20 estimating prokaryotic diversity. However,
measure abundances, so do not know the species– Log (bacterial abundance) strains or isolates with identical 16S rRNA
2
area curve, so we cannot estimate diversity. b Individuals curve gene sequences can have different physiolog-
In the absence of data, we can assume that a ical characteristics of ecological importance
N
particular distribution, for example a log-normal max and methods with greater taxonomic resolu-
distribution, applies. We can then make an tion are therefore required. Approaches
estimate on that basis. Guessing distributions is 20,21
not a wholly satisfactory procedure. Consequently, such as pyrosequencing , which address
others have sought to fit a line to, and extrapolate Area under individuals curve = N diversity across entire metagenomes, might
t be appropriate and could suggest alterna-
from, abundance data (typically clone libraries)
17 tive conceptual approaches to diversity.
available to them .
Unfortunately, clone libraries in microbial Number of individuals Many ecological questions require infor-
3 mation on specific phylogenetic groups
ecology are so small (<10 ) and microbial
communities so large (>1015) that the sample or functional groups, such as rhizobia or
distribution is unlikely to look like the 0 5 10 15 20 ammonia oxidizers, which might increase
community from which it was drawn. An Log (bacterial abundance) tractability.
alternative approach to estimating species 2 Many of the key questions in microbial
abundance curves is to examine the community ecology require reliable estima-
17
reassociation kinetics of DNA extracted from an environment . This approach involves tion of species richness. Analysis of species
denaturing DNA, separating the two strands of the DNA molecule, and then allowing them to abundance curves and the lack of a universal
reassociate. The most abundant sequences should reassociate first and the reassociation definition of species highlight the practical
kinetics therefore reflect the underlying distribution of similar sequences and, consequently, and conceptual difficulties associated with
the genomic diversity. However, for experimental reasons, only the reassociation of a small such estimates. The analyses described
proportion of the diversity can be observed. Consequently, the bulk of the curve is extrapolated
from a few taxa. It can be plausibly argued that this means that there is a great deal of above provide the basis for quantifying
uncertainty about the unobserved portion of the species abundance curve. species richness and for assessing the cost
The figure shows a log-normal species abundance curve and corresponding cumulative individuals and feasibility of quantification.
curve. 1/a is the width of the species curve, where a is the spread parameter. N is the abundance of
min
the least abundant species; N is the abundance of the most abundant species; and N is the modal Spatial scale
max 0
species abundance. Figure reproduced with permission from REF. 16 © (2002) US National Academy The pivotal role of spatial patterns and
of Sciences. processes in ecology is widely recognized.
Many systems, such as fragmented habitats
colleagues12 discussed the conditions for describe microbial diversity within any and populations, cannot be studied without
plasmid maintenance, and a recent theoreti- given environment. The sheer complex- a serious consideration of space. This has
cal exploration concludes that the evolu- ity of most environments, and the rapid generated the subdiscipline of landscape
tionary arms race between bacteria and realization that collectors curves of cloned ecology (which has recently been applied
bacteriophages can result in speciation of environmental 16S rRNA gene sequences to ecological aspects of antibiotic resistance
13 22
the host . This presents a major challenge to would give complete coverage only in the in bacteria ), the metapopulation paradigm
23,24
those studying prokaryotic population and very simplest ecosystems, has necessitated and metacommunity theory . Other
community ecology. The current solution is the development of a more theoretical basis research areas focus directly on the role
to use operational definitions of taxonomic for estimating prokaryotic diversity. To this of spatial scaling in ecological patterns.
units but we are a long way from a coherent end, Dunbar and colleagues15 and Curtis For example, species–area relationships
16
body of theory that relates the fluid nature of and colleagues pioneered the use of species (SARs) have a long history in ecology (see
bacterial genomes to the ecology of bacterial abundance curves that use log-normal rela- for example REFS 25–27). A SAR describing
communities. tionships (which will include some taxa that areas with relatively few species in com-
28
are rare and others that are present in high mon has greater species turnover and is
Measuring diversity and species richness numbers) to provide theoretical estimates steeper than a SAR with more species in
Since the estimation of substantial micro- of prokaryotic diversity, yielding diversity common; steepness therefore describes
14
bial diversity within soils , microbial estimates that are similar to those derived by how quickly local assemblages of species
ecologists have yearned to quantify and Torsvik and colleagues14 using DNA–DNA differentiate in space.
386 | MAY 2007 | VOLUME 5 © 2007 Nature Publishing Group www.nature.com/reviews/micro
PERSPECTIVES
The spatial scaling of microbial diversity increased and decreased taxonomic diver- in some instances resemble that of plants
is now being addressed by coupling the sity of bacteria in aquatic mesocosms and and animals. Further studies are required
molecular characterization of microbial that the shape of the relationship between to determine the mechanisms underlying
communities with macroecological theory29. productivity and diversity differed between microbial species richness and the influence
Compared with plants and animals, few SAR bacterial taxa. These initial results suggest of nutrient supply (for example, that associ-
studies have been published for microorgan- that bacterial diversity can vary with energy ated with eutrophication) on microbial species
isms, making a balanced comparison of and that the nature of the relationship can richness and diversity.
SAR patterns between the different groups
difficult. The SAR is commonly assumed Box 2 | Theoretical approaches for estimating microbial species
area relationships
z
to follow a power-law of the form S ∝ A ,
where S is species richness, A is area and z Contiguous habitats Islands
is the slope of the curve. Empirical evidence 0.3
suggests that for animals and plants within
contiguous habitats, z is generally in the
range of 0.1 to 0.2, and for discrete islands z
is steeper (0.2 < z < 0.39) (REF. 27), although
a new meta-analysis of SAR slopes sug- )0.2
gests that this difference might not be as z
30
pronounced as previously thought (BOX 2). Slope (
This study also confirmed a general trend in
the increasing steepness of z with increasing 0.1
body size from ciliates to large mammals.
Recent research has documented power-law
species–area (or more generally, taxa–area)
31,32 0.0
relationships in fungi and bacteria or k
29,33–36 sh ct e tan ls
and bacteria in island habitats . The a oil a a a a p
ants e e eehol ants
eri oms es eri eri r eri um eria pl
z values estimated in studies of contiguous Saltmar t t Anima
Marine Marine Animals Lak Bior T S
ct a Arid s a ct ct ct ct
habitats were much lower than those of ba di fungi cili and pl ba ba ba ba and
island habitats, but island z values were simi- Despite the theoretical and practical importance of species–area relationships (SARs), which
lar in magnitude to those observed for plants relate an area (A) to the number of species (S) found within this area, they are difficult to quantify
and animals. More research is required directly at ecologically relevant scales (see figure for a comparison of some microbial SARs from
to establish whether microorganisms are different contiguous habitats and islands). For organisms with the extraordinary abundance and
distributed spatially in ways that are similar diversity of microorganisms, this poses a challenge even at the scale of a single environmental
to plant and animal species, but one study sample. Microbial ecologists (and plant and animal ecologists) must therefore use theoretical
indicates that soil community composition is approaches to estimate SARs.
non-random at a continental scale, and that The most straightforward analyses of microbial SARs are direct plots of sample data (see for
example
soil community composition and diversity REF. 35). These analyses assume that the slope of the observed sample SAR parallels the
at large scales can be predicted primarily on slope that would result from a complete census. For a power-law SAR (in which the number of
z
37 species is a constant power of the area (S ∝ A ; where z is the slope of the curve)), this translates to
the basis of a single variable (pH) . Such an assumption that the observed species richness in a sample is a constant proportion of the total
patterns differ from those of plants and species richness in the area from which it was sampled, and that this constant proportion is not
animals, the biogeographical distributions affected by scale.
of which are influenced by site temperature Parametric approaches are also commonly used to estimate the increase of species richness
and latitude. with sample size (or sampling area) (BOX 1). In short, sample data are fitted to models of
relative abundance (or assumed on theoretical grounds), and this sample frequency
Diversity
energy relationships distribution is projected to estimate the number of unobserved species in the community70.
In addition to relationships between diver- Parametric approaches assume that the sample frequency distribution is a truncated version
sity and area, common patterns have been of the community-level distribution, which in turn assumes that individuals are randomly
described between diversity and energy. sampled from the community. In many studies this assumption can be seriously violated.
For example, primary productivity (the Microbial communities are commonly investigated by identifying individuals from soil or
rate of energy capture and carbon fixa- sediment cores across a landscape. Even if these environmental samples are randomly
tion by primary producers) is thought to distributed in space, spatial aggregation in microbial populations will result in a non-random
be a key determinant of plant and animal sample of individuals from the community.
An alternative approach to estimating SARs is to examine patterns of community turnover
27,38
biodiversity . A positive quadratic or across a landscape (the distance–decay relationship). This method has been applied to estimate
hump-shaped relationship is frequently SARs at local, regional and global scales (reviewed in REF. 29). Recent studies have shown that
71
observed between productivity and diversity, distance–decay methods underestimate SAR slopes , which suggests the need for further
in which diversity peaks at intermediate theoretical work in this area.
27 32
productivity , although other patterns have The figure shows the slopes of the SARs for contiguous habitat studies of saltmarsh bacteria ,
72 29 72
39,40 marine diatoms , arid soil fungi , and marine ciliates compared with the slopes of the SARs for
also been observed . Bacterial communi- 36 34
ties also exhibit such diversity–energy rela- island habitat studies of lake bacteria , wastewater treatment bioreactor bacteria , treehole
35 33
tionships. Horner-Devine and colleagues41 bacteria and coolant sump tank bacteria . The blue bars show typical values for studies of
26
observed that increasing productivity both animals and plants in these two habitats .
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