Embracing Community Ecology in Plant Microbiome Research

Dini‐Andreote, Francisco; Raaijmakers, Jos M.

doi:10.1016/j.tplants.2018.03.013

Cited by 69 publications

(57 citation statements)

References 11 publications

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“…For instance, outside of a host, differences in the climate, soils, and vegetation affect which microbes survive in the environment, and in turn, which microbes have the opportunity to colonize a primate's intestinal tract (this process is also known as species sorting; Székely & Langenheder, ). Within the host, across developmental time scales, microbial selection is thought to increase from early life to adulthood, partly due to physiochemical maturation of the gut, but also because hosts become more effective at curating their microbiomes (figure 2; Burns et al, ; Dini‐Andreote & Raaijmakers, ). Dietary regimes and gut morphology also represent strong selective forces (David et al, ; Groussin et al, ; Ley et al, ; McKenney et al, ).…”

Section: What Ecological Processes Contribute To Gut Microbiome Assemmentioning

confidence: 99%

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Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

Björk

Dasari

Grieneisen

et al. 2019

American J Primatol

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To date, most insights into the processes shaping vertebrate gut microbiomes have emerged from studies with cross-sectional designs. While this approach has been valuable, emerging time series analyses on vertebrate gut microbiomes show that gut microbial composition can change rapidly from 1 day to the next, with consequences for host physical functioning, health, and fitness. Hence, the next frontier of microbiome research will require longitudinal perspectives. Here we argue that primatologists, with their traditional focus on tracking the lives of individual animals and familiarity with longitudinal fecal sampling, are well positioned to conduct research at the forefront of gut microbiome dynamics. We begin by reviewing some of the most important ecological processes governing microbiome change over time, and briefly summarizing statistical challenges and approaches to microbiome time series analysis. We then introduce five questions of general interest to microbiome science where we think fieldbased primate studies are especially well positioned to fill major gaps: (a) Do early life events shape gut microbiome composition in adulthood? (b) Do shifting social landscapes cause gut microbial change? (c) Are gut microbiome phenotypes heritable across variable environments? (d) Does the gut microbiome show signs of host aging? And (e) do gut microbiome composition and dynamics predict host health and fitness?For all of these questions, we highlight areas where primatologists are uniquely positioned to make substantial contributions. We review preliminary evidence, discuss possible study designs, and suggest future directions. Research Highlights• To date nearly all insights into the processes shaping vertebrate gut microbiomes have emerged from studies that have cross-sectional designs, but emerging time series analyses show that gut microbiomes can change rapidly from 1 day to the next.• Field-based primate studies, owing to their focus on the lives of individual animals, and the relative ease of collecting longitudinal fecal samples from known animals, are better positioned to collect these data than studies of humans or other species.• We propose five questions of general interest to microbiome science where fieldbased primate studies are especially well positioned to fill major gaps. We review preliminary evidence, discuss possible study designs, and suggest future directions.Am J Primatol. 2019;81:e22970.wileyonlinelibrary.com/journal/ajp

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Section: What Ecological Processes Contribute To Gut Microbiome Assemmentioning

confidence: 99%

“…As microbial species persist across host development, the chances for speciation increase; hence speciation may play a stronger role in adult microbiomes as compared with infants and young juveniles. Figure adapted from Dini‐Andreote and Raaijmakers ()…”

Section: Key Areas Of Microbiome Science Where Primate Studies Can Comentioning

confidence: 99%

Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

Björk

Dasari

Grieneisen

et al. 2019

American J Primatol

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“…1a,e). Second the MiCRM incorporates stochasticity in dispersal and colonization [15][16][17][18]. Due to proximity effects, it is known that new environments are almost always colonized by only a subset of all the species capable of existing in that environment [19].…”

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A minimal model for microbial biodiversity can reproduce experimentally observed ecological patterns

Marsland

Cui

Mehta

2020

Sci Rep

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Surveys of microbial biodiversity such as the Earth Microbiome Project (EMP) and the Human Microbiome Project (HMP) have revealed robust ecological patterns across different environments.A major goal in ecology is to leverage these patterns to identify the ecological processes shaping microbial ecosystems. One promising approach is to use minimal models that can relate mechanistic assumptions at the microbe scale to community-level patterns. Here, we demonstrate the utility of this approach by showing that the Microbial Consumer Resource Model (MiCRM) -a minimal model for microbial communities with resource competition, metabolic crossfeeding and stochastic colonization -can qualitatively reproduce patterns found in survey data including compositional gradients, dissimilarity/overlap correlations, richness/harshness correlations, and nestedness of community composition. By using the MiCRM to generate synthetic data with different environmental and taxonomical structure, we show that large scale patterns in the EMP can be reproduced by considering the energetic cost of surviving in harsh environments and HMP patterns may reflect the importance of environmental filtering in shaping competition. We also show that recently discovered dissimilarity-overlap correlations in the HMP likely arise from communities that share similar environments rather than reflecting universal dynamics. We identify ecologically meaningful changes in parameters that alter or destroy each one of these patterns, suggesting new mechanistic hypotheses for further investigation. These findings highlight the promise of minimal models for microbial ecology. *

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“…Accordingly, studies are often designed and interpreted with either the plant as the active member which recruits its microbes (Gehring and Whitham, 1994) or the host plant as a background variable (e.g., "plant genotype") or a habitat. Instead, both the plant and associated microbes should be taken into account as active members of the interaction (Saikkonen et al, 1999;Bulgarelli et al, 2012;Dini-Andreote and Raaijmakers, 2018). This requires developing true dialogue, reciprocal understanding, and mutual collaboration between researchers from different life science fields.…”

Section: Future Perspectivesmentioning

confidence: 99%

Toward Comprehensive Plant Microbiome Research

2020

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Microbes have driven eco-evolutionary adaptations organizing biodiversity from the origin of life. They are ubiquitous and abundant, facilitating the biochemical processes that make Earth habitable and shape ecosystem structures, functions, and services. Recent studies reveal that commensalistic and beneficial microbes associated with wild and domesticated plants may aid in establishing sustainable agriculture for a changing climate. However, developing microbe-based biotechnologies and ecosystem services requires a thorough understanding of the diversity and complexity of microbial interactions with each other and with higher organisms. We discuss the hot and blind spots in contemporary research on plant microbiomes, and how the latest molecular biological techniques and empirical eco-evolutionary approaches could elevate our perception of microbe-plant interactions through multidisciplinary studies.

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Embracing Community Ecology in Plant Microbiome Research

Cited by 69 publications

References 11 publications

Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

A minimal model for microbial biodiversity can reproduce experimentally observed ecological patterns

Toward Comprehensive Plant Microbiome Research

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