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Microbes are the unseen majority in soil and comprise a large portion of lifes genetic diversity. Despite their abundance, the impact of soil microbes on ecosystem processes is still poorly understood. Here we explore the various roles that soil microbes play in terrestrial ecosystems with special emphasis on their contribution to plant productivity and diversity. Soil microbes are important regulators of plant productivity, especially in nutrient poor ecosystems where plant symbionts are responsible for the acquisition of limiting nutrients. Mycorrhizal fungi and nitrogenfixing bacteria are responsible for c. 5‐20% (grassland and savannah) to 80% (temperate and boreal forests) of all nitrogen, and up to 75% of phosphorus, that is acquired by plants annually. Free-living microbes also strongly regulate plant productivity, through the mineralization of, and competition for, nutrients that sustain plant productivity. Soil microbes, including microbial pathogens, are also important regulators of plant community dynamics and plant diversity, determining plant abundance and, in some cases, facilitating invasion by exotic plants. Conservative estimates suggest that c. 20 000 plant species are completely dependent on microbial symbionts for growth and survival pointing to the importance of soil microbes as regulators of plant species richness on Earth. Overall, this review shows that soil microbes must be considered as important drivers of plant diversity and productivity in terrestrial ecosystems.

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The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

Bacterial biofilms are formed by communities that are embedded in a self-produced matrix of extracellular polymeric substances (EPS). Importantly, bacteria in biofilms exhibit a set of 'emergent properties' that differ substantially from free-living bacterial cells. In this Review, we consider the fundamental role of the biofilm matrix in establishing the emergent properties of biofilms, describing how the characteristic features of biofilms - such as social cooperation, resource capture and enhanced survival of exposure to antimicrobials - all rely on the structural and functional properties of the matrix. Finally, we highlight the value of an ecological perspective in the study of the emergent properties of biofilms, which enables an appreciation of the ecological success of biofilms as habitat formers and, more generally, as a bacterial lifestyle.

Biofilms: an emergent form of bacterial life.

We review the biogeography of microorganisms in light of the biogeography of macroorganisms A large body of research supports the idea that free-living microbial taxa exhibit biogeographic patterns Current evidence confirms that, as proposed by the Baas-Becking hypothesis, 'the environment selects' and is, in part, responsible for spatial variation in microbial diversity However, recent studies also dispute the idea that 'everything is everywhere' We also consider how the processes that generate and maintain biogeographic patterns in macroorganisms could operate in the microbial world

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Microbial biogeography : putting microorganisms on the map

Metagenomics and 16S pyrosequencing have enabled the study of ecosystem structure and dynamics to great depth and accuracy. Co-occurrence and correlation patterns found in these data sets are increasingly used for the prediction of species interactions in environments ranging from the oceans to the human microbiome. In addition, parallelized co-culture assays and combinatorial labelling experiments allow high-throughput discovery of cooperative and competitive relationships between species. In this Review, we describe how these techniques are opening the way towards global ecosystem network prediction and the development of ecosystem-wide dynamic models.

Microbial interactions: from networks to models

A central goal in microbial ecology is to simplify the extraordinary biodiversity that inhabits natural environments into ecologically coherent units. We profiled (16S rRNA sequencing)  > 700 semi-aquatic bacterial communities while measuring their functional capacity when grown in laboratory conditions. This approach allowed us to investigate the relationship between composition and function excluding confounding environmental factors. Simulated data allowed us to reject the hypothesis that stochastic processes were responsible for community assembly, suggesting that niche effects prevailed. Consistent with this idea we identified six distinct community classes that contained samples collected from distant locations. Structural equation models showed there was a functional signature associated with each community class. We obtained a more mechanistic understanding of the classes using metagenomic predictions (PiCRUST). This approach allowed us to show that the classes contained distinct genetic repertoires reflecting community-level ecological strategies. The ecological strategies resemble the classical distinction between r- and K-strategists, suggesting that bacterial community assembly may be explained by simple ecological mechanisms. Metagenome approaches can unravel relationships between environment, community composition, and ecological functions. Here, the authors show that bacterial communities sampled from rainwater pools can be clustered into few classes with distinct functional capacities and genetic repertoires, the assembly of which is likely driven by local conditions.

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Community-level signatures of ecological succession in natural bacterial communities.

Recent theory and experiments have reported a reproducible tendency for the coexistence of microbial species under controlled environmental conditions. This observation has been explained in the context of competition for resources and metabolic complementarity given that, in microbial communities (MCs), many excreted by-products of metabolism may also be resources. MCs therefore play a key role in promoting their own stability and in shaping the niches of the constituent taxa. We suggest that an intermediate level of organization between the species and the community level may be pervasive, where tightly knit metabolic interactions create discrete consortia that are stably maintained. We call these units Metabolically Cohesive Consortia (MeCoCos) and we discuss the environmental context in which we expect their formation, and the ecological and evolutionary consequences of their existence. We argue that the ability to identify MeCoCos would open new avenues to link the species-, community- and ecosystem-level properties, with consequences for our understanding of microbial ecology and evolution, and an improved ability to predict ecosystem functioning in the wild. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0245

Metabolically cohesive microbial consortia and ecosystem functioning

We studied territoriality and habitat use by yellow phase juvenile blue tangs, Acanthurus coeruleus, on a small fringing reef in Barbados, West Indies. Juvenile blue tangs occurred on the reef crest, spurs, and a transition zone between the reef crest and reef flat at a density of about 8 individuals per 100 m2, but were much rarer on the reef flat. They were solitary and occupied stable home ranges (median=0.85 m2) that increased with body size. Observational and experimental data documented aggressive defense of home ranges against conspecific and to a lesser extent congeneric, A. bahianus, juveniles (about 7.5 approaches and attacks per hour directed at intruders). Home range locations were structurally more complex and closer to a vertical face than expected by chance. Although juvenile blue tang territories overlapped considerably with those of larger and more aggressive Stegastes damselfish, which are believed to exclude solitary adult Acanthurus spp. from reef crest and spurs, the tangs avoided Stegastes and were rarely chased (<0.3 fleeing events per hour). Space use and social organization of yellow juvenile blue tangs contrast strikingly with that of both conspecific adults and congeneric juveniles.

Territoriality and Habitat Use by Juvenile Blue Tangs, Acanthurus coeruleus

Antibiotics leak constantly into environments due to widespread use in agriculture and human therapy. Although sublethal concentrations are well known to select for antibiotic-resistant bacteria, little is known about how bacterial evolution cascades through food webs, having indirect effect on species not directly affected by antibiotics (e.g. via population dynamics or pleiotropic effects). Here, we used an experimental evolution approach to test how temporal patterns of antibiotic stress, as well as migration within metapopulations, affect the evolution and ecology of microcosms containing one prey bacterium, one phage and two protist predators. We found that environmental variability, autocorrelation and migration had only subtle effects for population and evolutionary dynamics. However, unexpectedly, bacteria evolved greatest fitness increases to both antibiotics and enemies when the sublethal levels of antibiotics were highest, indicating positive pleiotropy. Crucially, bacterial adaptation cascaded through the food web leading to reduced predator-to-prey abundance ratio, lowered predator community diversity and increased instability of populations. Our results show that the presence of natural enemies can modify and even reverse the effects of antibiotics on bacteria, and that antibiotic selection can change the ecological properties of multitrophic microbial communities by having indirect effects on species not directly affected by antibiotics.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2014.2920

Bacterial adaptation to sublethal antibiotic gradients can change the ecological properties of multitrophic microbial communities

Species interactions can play a major role in shaping evolution in new environments. In theory, species interactions can either stimulate evolution by promoting coevolution or inhibit evolution by constraining ecological opportunity. The relative strength of these effects should vary as species richness increases, and yet there has been little evidence for evolution of component species in communities. We evolved bacterial microcosms containing between 1 and 12 species in three different environments. Growth rates and yields of isolates that evolved in communities were lower than those that evolved in monocultures, consistent with recent theory that competition constrains species to specialize on narrower sets of resources. This effect saturated or reversed at higher levels of richness, consistent with theory that directional effects of species interactions should weaken in more diverse communities. Species varied considerably, however, in their responses to both environment and richness levels. Mechanistic models and experiments are now needed to understand and predict joint evolutionary dynamics of species in diverse communities.

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Thomas Bell

Papers

Community-level signatures of ecological succession in natural bacterial communities.

Metabolically cohesive microbial consortia and ecosystem functioning

Territoriality and Habitat Use by Juvenile Blue Tangs, Acanthurus coeruleus

Bacterial adaptation to sublethal antibiotic gradients can change the ecological properties of multitrophic microbial communities

Saturating effects of species diversity on life-history evolution in bacteria