Review

Microbiomes in light of traits: A phylogenetic perspective

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Science  06 Nov 2015:
Vol. 350, Issue 6261, aac9323
DOI: 10.1126/science.aac9323

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Function in the tree of life

How does the composition of microbial communities integrate functionally with the wider environment? Martiny et al. review how patterns of microbial species abundances in different environments and disease states can have strong evolutionary signals. Some environmental changes select the survival of organisms with conserved metabolisms requiring complex configurations of proteins and cofactors that have long evolutionary histories, such as methane producers. In contrast, surviving antibiotic exposure may only require a single gene that can be traded promiscuously among many unrelated organisms. So, depending on the key ingredient (whether it is temperature, light, nutrient, or a dose of antibiotic) and the evolutionary history of its complementary metabolism, shifting environmental conditions will have predictable effects at different levels within the microbial tree of life.

Science, this issue p. 10.1126/science.aac9323

Structured Abstract

BACKGROUND

Microbial communities—microbiomes—are intricately linked to human health and critical ecosystem services. New technologies allow the rapid characterization of hundreds of samples at a time and provide a sweeping perspective on microbiome patterns. However, a systematic understanding of what determines microbiome diversity and composition and its implications for system functioning is still lacking. A focus on the phenotypic characteristics of microorganisms—their traits—offers a path for interpreting the growing amount of microbiome data. Indeed, a variety of trait-based approaches have been proposed for plants and animal communities, and this approach has helped to clarify the mechanisms underlying community assembly, diversity-process relationships, and ecosystem responses to environmental change.

Although there is a growing emphasis on microbial traits, the concept has not been fully appreciated in microbiology. However, a trait focus for microorganisms may present an even larger research opportunity than for macro-organisms. Not only do microorganisms play a central role in nutrient and energy cycling in most systems, but the techniques used to characterize microbiomes usually provide extensive molecular and phylogenetic information.

ADVANCES

One major difference between macro- and microorganisms is the potential for horizontal gene transfer (HGT) in microbes. Higher rates of HGT mean that many microbial traits might be unrelated to the history of the vertically descended parts of the genome. If true, then the taxonomic composition of a microbiome might reveal little about the health or functioning of a system. We first review key aspects of microbial traits and then recent studies that document the distribution of microbial traits onto the tree of life. A synthesis of these studies reveals that, despite the promiscuity of HGT, microbial traits appear to be phylogenetically conserved, or not distributed randomly across the tree of life. Further, microbial traits appear to be conserved in a hierarchical fashion, possibly linked to their biochemical and genetic complexity. For instance, traits such as pH and salinity preference are relatively deeply conserved, such that taxa within deep clades tend to share the trait. In contrast, other traits like the ability to use simple carbon substrates or to take up organic phosphorus are shallowly conserved, and taxa share these traits only within small, shallow clades.

OUTLOOK

The phylogenetic, trait-based framework that emerges offers a path to interpret microbiome variation and its connection to the health and functioning of environmental, engineered, and human systems. In particular, the taxonomic resolution of biogeographic patterns provides information about the traits under selection, even across entirely different systems. Parallels observed among human and free-living communities support this idea. For instance, microbial traits related to growth on different substrates (e.g., proteins, fats, and carbohydrates) in the human gut appear to be conserved at approximately the genus level, a resolution associated with the level of conservation of glycoside hydrolase genes in bacteria generally. A focus on two particular types of traits—response and effect traits—may also aid in microbiome management, whether that means maintaining human health or mitigating climate change impacts. Future work on microbial traits must consider three challenges: the influence of different trait measurements on cross-study comparisons; correlations between traits within and among microorganisms; and interactions among microbial traits, the environment, and other organisms. Our conclusions also have implications for the growing field of community phylogenetics beyond applications to microorganisms.

Measuring and mapping the phylogenetic distribution of microbial traits.

Microbial traits encompass a range of phenotypic characteristics that vary in complexity, including (clockwise from top) virus resistance, cellulose degradation, salinity preference, nitrogen fixation, biofilm formation, and the production of alkaline phosphatase. Each trait can be measured in innumerable ways. For instance, it can be described by discrete or continuous metrics (e.g., the presence of a gene versus the number of gene copies) of potential or realized phenotypes (e.g., those assayed by functional metagenomics versus in situ activity).

[Credits: C. Wiehe; M. Maltz; J. Martiny; L. Riemann; J. Haagensen; K. Frischkorn]

Abstract

A focus on the phenotypic characteristics of microorganisms—their traits—offers a path for interpreting the growing amount of microbiome data. We review key aspects of microbial traits, as well as approaches used to assay their phylogenetic distribution. Recent studies reveal that microbial traits are differentially conserved across the tree of life and appear to be conserved in a hierarchical fashion, possibly linked to their biochemical complexity. These results suggest a predictive framework whereby the genetic (or taxonomic) resolution of microbiome variation among samples provides information about the traits under selection. The organizational parallels seen among human and free-living microbiomes seem to support this idea. Developments in this framework may offer predictions not only for how microbial composition responds to changing environmental conditions, but also for how these changes may alter the health or functioning in human, engineered, and environmental systems.

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