Beyond biogeographic patterns: processes shaping the microbial landscape

Key Points

  • Biogeography is the study of the distribution of organisms and the ecological and evolutionary processes that shape those distributions. Over the past decade, microbiologists have established the existence of biogeographic patterns among a wide variety of microorganisms, and interest is now shifting towards identifying the mechanisms that shape these patterns.

  • Traditionally, mechanisms that shape the composition and diversity within species are considered to be evolutionary processes, and those that shape the composition and diversity among species are considered to be ecological processes. However, microbial biogeography studies often characterize diversity along a continuous scale of taxonomic resolution using the nucleotide sequences of a single marker gene. In this case, the boundary between ecological and evolutionary processes is particularly blurry. Hence, we merge concepts from both fields to describe the processes that shape microbial biogeographic patterns.

  • Here, we propose a theoretical framework that describes just four processes — selection, drift, dispersal and mutation — which interact to create and maintain microbial biogeographic patterns at all taxonomic scales. As an illustrative example, we show how these processes shape the most commonly studied biogeographic pattern: the distance–decay relationship.

  • We carried out a literature review to assess the evidence for the relative importance of these processes in shaping microbial biogeographic patterns. Although selection imposed by current environmental factors had the strongest influence on microbial spatial distributions, historical processes driven by dispersal limitation also influenced the distribution of at least some microorganisms from all domains of life and from various habitat types, spatial scales and taxonomic resolutions.

  • As different combinations of the same four processes can interact to create the same pattern, we conclude that it remains difficult to disentangle the relative importance of selection, drift, dispersal and mutation by analysing distance–decay patterns alone. We suggest that the field might advance by emphasizing process over pattern: tailoring studies to detect and evaluate specific processes through manipulative experiments, temporal data sets and the incorporation of theoretical models.

Abstract

Recently, microbiologists have established the existence of biogeographic patterns among a wide range of microorganisms. The focus of the field is now shifting to identifying the mechanisms that shape these patterns. Here, we propose that four processes — selection, drift, dispersal and mutation — create and maintain microbial biogeographic patterns on inseparable ecological and evolutionary scales. We consider how the interplay of these processes affects one biogeographic pattern, the distance–decay relationship, and review evidence from the published literature for the processes driving this pattern in microorganisms. Given the limitations of inferring processes from biogeographic patterns, we suggest that studies should focus on directly testing the underlying processes.

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Figure 1: The sliding scale of microbial taxonomic definitions and its influence on microbial biogeographic patterns.
Figure 2: The effect of the four processes on the relationship between compositional similarity and spatial distance.
Figure 3: Studies reporting a significant correlation between microbial composition and spatial distance or an environmental variable.
Figure 4: Explained variance in microbial composition.

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Acknowledgements

The authors thank A. Martiny, S. Allison, A. Amend, L. Crummett, K. Whiteson, A. Durbin, K. Matulich, S. Kivlin, N. Hynson and J. Talbot for feedback and discussions. This work was supported by a US National Oceanic and Atmospheric Administration–National Estuarine Research Reserve System (NOAA–NERRS) Graduate Research Fellowship to C.A.H. and a US National Science Foundation Grant (OCE-1031783) to J.B.H.M.

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Correspondence to China A. Hanson or Jennifer B. H. Martiny.

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Glossary

Richness

The number of taxa in a sample, assemblage or community.

Composition

The identity and relative abundance of taxa in a sample, assemblage or community.

Taxonomic resolution

The level of genetic variation of the taxa considered.

Taxon

A group into which related organisms are classified. For microorganisms, taxa are usually defined by sequence similarity of one or more genomic regions. This includes the possibility that taxa are defined by entirely unique genomes (at the highest genetic resolution possible).

Community

All individuals of a defined set of many taxa within an area (for instance, all bacterial taxa).

Taxonomic breadth

The extent of taxa considered.

Cosmopolitan

Having a widespread distribution, present almost everywhere.

Horizontal gene transfer

Transfer of genetic material between independent organisms other than transfer by direct decent.

Environment effect

A correlation of biotic composition with measured environmental variables after controlling for the influence of geographic distance.

Distance effect

A correlation of biotic composition with geographic distance after controlling for the influence of the contemporary environment.

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Hanson, C., Fuhrman, J., Horner-Devine, M. et al. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10, 497–506 (2012). https://doi.org/10.1038/nrmicro2795

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