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Data and code for "Macroevolutionary constraints on global microbial diversity"

Dormancy is as an adaptation to living in fluctuating environments. It can also influence species interactions, for example, by providing organisms with a refuge from predators and parasites. Here we test the hypothesis that dormancy generates a seed bank of protected individuals that can modify antagonistic coevolutionary dynamics. We experimentally evolved a spore-forming bacterial host along with a phage parasite that can infect active but not dormant cells. Seed banks buffered population dynamics against phage infection and retained phenotypic diversity that was otherwise lost to directional selection. By storing genetic diversity, seed banks also altered the distribution of host alleles, which contributed to dampened coevolutionary dynamics. Our findings demonstrate that dormancy generates a seed bank that can modify the eco-evolutionary outcomes of host-parasite systems.

Microbes can promote beneficial plant and animal responses to abiotic environments, but the ecological drivers of this benefit remain elusive. Here we investigated byproduct benefits, which occur when traits that increase the fitness of one species provide incidental benefits to another species with no direct cost to the provider species. In experimental mesocosms, microbial traits predicted plant responses to soil moisture such that bacteria with self-beneficial traits in drought increased plant early growth, size at reproduction, and chlorophyll concentration under drought, while bacteria with self-beneficial traits in well-watered environments increased these same plant traits in well-watered environments. Thus, microbial traits that promote microbial success in different soil moisture environments also promote plant success in these same environments. Our results show that the concept of byproduct benefits, originally conceived to explain the evolution of cooperation in pairwise mutualisms, also applies to interactions between plants and non-symbiotic soil microbes.

Dissolved organic matter (DOM) is a large and complex mixture of molecules that fuels microbial metabolism and regulates biogeochemical cycles. Individual DOM molecules have unique functional traits, but how their assemblages vary deterministically under global change remains poorly understood. Here, we examine DOM and associated bacteria in 300 aquatic microcosms deployed on mountainsides that span contrasting temperatures and nutrient gradients. Based on molecular trait dimensions of reactivity and activity, we partition the DOM composition into labile-active, recalcitrant-active, recalcitrant-inactive, and labile-inactive fractions and quantify the relative influences of deterministic and stochastic processes governing the assembly of each. At both subtropical and subarctic study sites, the assembly of labile or recalcitrant molecules in active fractions is primarily governed by deterministic processes, while stochastic processes are more important for the assembly of molecules within inactive fractions. Surprisingly, the importance of deterministic selection increases with global change gradients for recalcitrant molecules in both active and inactive fractions, and this trend is paralleled by changes in the deterministic assembly of microbial communities and environmental filtering, respectively. Together, our results highlight the shift in focus from potential reactivity to realized activity and indicate that active and inactive fractions of DOM assemblages are structured by contrasting processes, and their recalcitrant components are consistently sensitive to global change. Our study partitions the DOM molecular composition across functional traits and links DOM with microbes via a shared ecological framework of assembly processes. This integrated approach opens new avenues to understand the assembly and turnover of organic carbon in a changing world.

Movement is critical for the fitness of organisms, both large and small. It dictates how individuals acquire resources, evade predators, exchange genetic material, and respond to stressful environments. Movement also influences ecological and evolutionary dynamics at scales beyond the individual organism. However, the links between individual motility and the processes that generate and maintain microbial diversity are poorly understood. Movement ecology is a framework linking the physiological and behavioral properties of individuals to movement patterns across scales of space, time, and biological organization. By synthesizing insights from cell biology, ecology, and evolution, we expand theory from movement ecology to predict the causes and consequences of microbial movements from small to large scales.

Organisms have evolved different mechanisms in response to periods of environmental stress, including dormancy – a reversible state of reduced metabolic activity. Transitions to and from dormancy can be random or induced by changes in environmental conditions. Prior theoretical work has shown that stochastic transitioning between active and dormant states at the individual level can maximize fitness at the population level. However, such theories of ‘bet-hedging’ strategies typically neglect certain physiological features of transitions to dormancy, including time lags to gain protective benefits. Here, we construct and analyze a dynamic model that couples stochastic changes in environmental state with the population dynamics of organisms that can initiate dormancy after an explicit time delay. Stochastic environments are simulated using a multi-state Markov chain through which the mean and variance of environmental residence time can be adjusted. In the absence of time lags (or in the limit of very short lags), we find that bet-hedging strategy transition probabilities scale inversely with the mean environmental residence times, consistent with prior theory. We also find that increasing delays in dormancy decreases optimal transitioning probabilities, an effect that can be influenced by the correlations of environmental noise. When environmental residence times - either good or bad - are uncorrelated, the maximum population level fitness is obtained given low levels of transitioning between active and dormant states. However when environmental residence times are correlated, optimal dormancy initiation and termination probabilities increase insofar as the mean environmental persistent time is longer than the delay to reach dormancy. We also find that bet hedging is no longer advantageous when delays to enter dormancy exceed the mean environmental residence times. Altogether, these results show how physiological limits to dormancy and environmental dynamics shape the evolutionary benefits and even viability of bet hedging strategies at population scales.

1.Rescue effects arise when ecological and evolutionary processes restore intrinsic positive growth rates in populations that are at risk of going extinct. Rescue effects have traditionally focused on the roles of immigration, phenotypic plasticity, gene flow, and adaptation. However, species interactions are also critical for understanding how populations respond to environmental change.2.In particular, the fitness of plant and animal hosts is strongly influenced by symbiotic associations with the bacteria, archaea, microeukaryotes, and viruses that collectively make up a host’s microbiome. While some are pathogenic, many microorganisms confer nutritional, immunological, and developmental benefits that can protect hosts against the effects of rapid environmental change. 3.Microbial rescue occurs when changes in microbiome abundance, composition, or activity influence host physiology or behavior in ways that improve host fitness. If these microbial attributes and their beneficial effects are transmitted through a population, it may stabilize growth rates and reduce the probability of extinction.4.In addition to providing a framework to guide theoretical and empirical efforts in host-microbiome research, the principles of microbial rescue may also be useful for adaptively managing at-risk species. We discuss the risks and rewards of incorporating microbial rescue into conservation strategies such as probiotics, assisted migration, and captive breeding.

By entering a reversible state of reduced metabolic activity, dormant microorganisms are able to tolerate suboptimal conditions that would otherwise reduce their fitness. Dormancy may also benefit bacteria by serving as a refuge from parasitic infections. Here we focus on dormancy in the Firmicutes, where endospore development is transcriptionally regulated by the expression of sigma factors. A disruption of this process could influence the survivorship and reproduction of phages that infect spore-forming hosts with implications for coevolutionary dynamics. Here, we characterized the distribution and diversity of sigma factors in nearly 3,500 phage genomes. Homologs of sporulation-specific sigma factors were identified in phages that infect spore-forming hosts. Unlike sigma factors required for phage reproduction, the sporulation-like sigma factors were non-essential for lytic infection. However, when expressed in the spore-forming Bacillus subtilis, sigma factors from phages activated the bacterial sporulation gene network and reduced spore yield. Our findings suggest that the acquisition of host-like transcriptional regulators may allow phages to manipulate a complex and ancient trait in one of the most abundant cell types on Earth.

Microbes play a critical role in regulating the size, composition, and turnover of dissolved organic matter (DOM), which is one of the largest pools of carbon in aquatic ecosystems. Global change may alter DOM-microbe associations with implications for biogeochemical cycles, although disentangling these complex interactions remains a major challenge. Here we develop a framework called Energy-Diversity-Trait integrative Analysis (EDTiA) to examine the associations between DOM and bacteria along temperature and nutrient gradients in a manipulative field experiment on mountainsides in contrasting subarctic and subtropical climates. In both study regions, the chemical composition of DOM correlated with bacterial communities, and was primarily controlled by nutrients and to a lesser degree by temperature. At a molecular-level, DOM-bacteria associations depended strongly on the molecular traits of DOM, with negative associations indicative of decomposition as molecules are more biolabile. Using bipartite networks, we further demonstrated that negative associations were more specialized than positive associations indicative of DOM production. Nutrient enrichment promoted specialization of positive associations, but decreased specialization of negative associations particularly at warmer temperatures in subtropical climate. These global change drivers influenced specialization of negative associations most strongly via molecular traits, while both molecular traits and bacterial diversity similarly affected positive associations. Together, our framework provides a quantitative approach to understand DOM-microbe associations and wider carbon cycling across scales under global change.

Fluctuations in the availability of resources constrains the growth and reproduction of individuals, which subsequently effects the evolution of their respective populations. Many organisms contend with such fluctuations by entering a reversible state of reduced metabolic activity, a phenomenon known as dormancy. This pool of dormant individuals (i.e., a seed bank) does not reproduce and is expected to act as an evolutionary buffer, though it is difficult to observe this effect directly over an extended evolutionary timescale. Through genetic manipulation, we analyze the molecular evolutionary dynamics of Bacillus subtilis populations in the presence and absence of a seed bank over 700 days. The ability of these bacteria to enter a dormant state increased the accumulation of genetic diversity over time and altered the trajectory of mutations, findings that were recapitulated using simulations based on a mathematical model of evolutionary dynamics. While the ability to form a seed bank did not alter the degree of negative selection, we found that it consistently altered the direction of molecular evolution across genes. Together, these results show that the ability to form a seed bank can affect the direction and rate of molecular evolution over an extended evolutionary timescale.

Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 populations in an effectively closed system for 1,000 d. All but one taxon survived prolonged resource scarcity, yielding estimated times to extinction ranging over four orders of magnitude from 100 to 105 y. Our findings corroborate reports of long-lived bacteria recovered from ancient environmental samples, while providing insight into mechanisms of persistence. As death rates declined over time, lifespan was extended through the scavenging of dead cells. Although reproduction was suppressed in the absence of exogenous resources, populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of purifying selection as well as molecular signals of adaptation. Consistent ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.

Across the tree of life, populations have evolved the capacity to contend with suboptimal conditions by engaging in dormancy, whereby individuals enter a reversible state of reduced metabolic activity. The resulting seed banks are complex, storing information and imparting memory that gives rise to multi-scale structures and networks spanning collections of cells to entire ecosystems. We outline the fundamental attributes and emergent phenomena associated with dormancy and seed banks, with the vision for a unifying and mathematically based framework that can address problems in the life sciences, ranging from global change to cancer biology., Seed banks are generated when individuals enter a dormant state, a phenomenon that has evolved among diverse taxa, but that is also found in stem cells, brains, and tumors. Here, Lennon et al. synthesize the fundamentals of seed-bank theory and the emergence of complex patterns and dynamics in mathematics and the life sciences.

Peatlands store one-third of Earth's soil carbon, the stability of which is uncertain due to climate change-driven shifts in hydrology and vegetation, and consequent impacts on microbial communities that mediate decomposition. Peatland carbon cycling varies over steep physicochemical gradients characterizing vertical peat profiles. However, it is unclear how drought-mediated changes in plant functional groups (PFGs) and water table (WT) levels affect microbial communities at different depths. We combined a multiyear mesocosm experiment with community sequencing across a 70-cm depth gradient, to test the hypotheses that vascular PFGs (Ericaceae vs. sedges) and WT (high vs. low) structure peatland microbial communities in depth-dependent ways. Several key results emerged. (i) Both fungal and prokaryote (bacteria and archaea) community structure shifted with WT and PFG manipulation, but fungi were much more sensitive to PFG whereas prokaryotes were much more sensitive to WT. (ii) PFG effects were largely driven by Ericaceae, although sedge effects were evident in specific cases (e.g., methanotrophs). (iii) Treatment effects varied with depth: the influence of PFG was strongest in shallow peat (0-10, 10-20 cm), whereas WT effects were strongest at the surface and middle depths (0-10, 30-40 cm), and all treatment effects waned in the deepest peat (60-70 cm). Our results underline the depth-dependent and taxon-specific ways that plant communities and hydrologic variability shape peatland microbial communities, pointing to the importance of understanding how these factors integrate across soil profiles when examining peatland responses to climate change.

Possessing only essential genes, a minimal cell can reveal mechanisms and processes that are critical for the persistence and stability of life. Here, we report on how a synthetically constructed minimal cell contends with the forces of evolution compared to a non-minimized cell from which it was derived. Genome streamlining was costly, but 80% of fitness was regained in 2000 generations. Although selection acted upon divergent sets of mutations, the rates of adaptation in the minimal and non-minimal cell were equivalent. The only apparent constraint of minimization involved epistatic interactions that inhibited the evolution of cell size. Together, our findings demonstrate the power of natural selection to rapidly optimize fitness in the simplest autonomous organism, with implications for the evolution of cellular complexity.

Conventional agricultural practices negatively impact soil biodiversity, carbon stocks, and greenhouse gas emissions in ways that make them unsustainable for supporting future supply of food and fiber. Better management of agrobiodiversity will likely play a critical role in transitioning towards more sustainable practices. In particular, innovation and developments targeting the aboveground and belowground components of agroecosystems should be informed by frameworks and approaches that harness the –in particular functional– diversity of complex microbial communities. Here, we review and discuss microbial trait-based approaches that will help us understand and steer agroecosystem functioning in the face of global change. We highlight how trait-based approaches can improve agricultural practices related to soil functioning (e.g. soil fertility and aggregation); climate regulation (e.g. carbon storage and greenhouse gas emissions) and adaptation to climate change; plant health; and reduction of contaminant-related hazards for human health. We also consider how microbial trait-based approaches can be used as a tool to improve cultivated plant performance through artificial selection and microbiome engineering. Last, we discuss the inherent obstacles associated with the development and implementation of trait-based approaches owing to strong interactions within microbial communities and linkages between plants and the soil environment. Despite these obstacles, microbial trait-based approaches hold promise for the sustainable management of agricultural ecosystems needed to feed and nourish a rapidly growing human population.

Microorganisms are strongly influenced by the bottom-up effects of resource supply. While many species respond to fluctuations in the concentration of resources, microbial diversity may also be affected by the heterogeneity of the resource pool, which often reflects a mixture of distinct molecules. To test this hypothesis, we examined resource–diversity relationships for bacterioplankton in a set of north temperate lakes that varied in their concentration and composition of dissolved organic matter (DOM), which is an important resource for heterotrophic bacteria. Using 16S rRNA transcript sequencing and ecosystem metabolomics, we documented strong relationships between bacterial alpha-diversity (richness and evenness) and the bulk concentration and the number of molecules in the DOM pool. Similarly, bacterial community beta-diversity was related to both DOM concentration and composition. However, in some lakes the relative abundance of resource generalists, which was inversely related to the DOM concentration, may have reduced the effect of DOM heterogeneity on community composition. Together, our results demonstrate the potential metabolic interactions between bacteria and organic matter and suggest that changes in organic matter composition may alter the structure and function of bacterial communities.

Coevolution arises from the reciprocal genetic change between species and represents a major evolutionary force that contributes to the generation and maintenance of biodiversity. The tempo and mode of coevolution are affected by environmental conditions that modify species interactions. For example, the scarcity of essential elements influences the nutrition and productivity of host populations, which should not only regulate parasite dynamics, but also drive the evolution of defense and virulence traits. To explore the effects of nutrient availability on antagonistic coevolution, we conducted a long-term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. Our manipulation of nutrient stoichiometry influenced the stability of host-parasite interactions, but also affected the underlying mode of coevolution. By assessing infectivity with more than 18,000 pairwise challenges using time-shift and network analyses, we documented directional selection for increased phage resistance, a pattern that is consistent with coevolutionary arms-race dynamics. In contrast, phage infectivity fluctuated through time, as expected when coevolution is determined by negative frequency-dependent selection, but was 70% higher on naive hosts that evolved under N-limitation versus P-limitation. Furthermore, infection networks were 25% more modular under P-limitation than N-limitation reflecting host-range contraction and an asymmetric coevolutionary trajectory. Together, our results demonstrate that nutrient stoichiometry creates eco-evolutionary feedbacks that may alter the dynamics and functioning of environmental and host-associated microbial communities.

Coexisting species often exhibit negative frequency dependence due to mechanisms that promote population growth and persistence when rare. These stabilising mechanisms can maintain diversity through interspecific niche differences, but also through life-history strategies like dormancy that buffer populations in fluctuating environments. However, there are few tests demonstrating how seed banks contribute to long-term community dynamics and the maintenance of diversity. Using a multi-year, high-frequency time series of bacterial community data from a north temperate lake, we documented patterns consistent with stabilising coexistence. Bacterial taxa exhibited differential responses to seasonal environmental conditions, while seed bank dynamics helped maintain diversity over less-favourable winter periods. Strong negative frequency dependence in rare, but metabolically active, taxa suggested a role for biotic interactions in promoting coexistence. Together, our results provide field-based evidence that niche differences and seed banks contribute to recurring community dynamics and the long-term maintenance of diversity in nature.

While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. However, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant-soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. In a factorially designed experiment, we then applied the Rpf to soil containing field mustard (Brassica rapa), an agronomically important plant species. Plant biomass was ~33% lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant-soil feedbacks in ways that affect above- and belowground biodiversity and function.

Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000 days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that although the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon.

As the most abundant and diverse form of life on Earth, microorganisms commonly inhabit energy-limited environments where cellular maintenance and growth is highly constrained. To gain insight into how microorganisms persist under such conditions, we derived demographic parameters from a diverse collection of bacteria by censusing 100 populations in a closed system for 1,000 days. All but one taxon survived prolonged resource scarcity, yielding estimated times-to-extinction ranging over four orders of magnitude from 100– 105years. These findings corroborate reports of long-lived bacteria that have been recovered from ancient environmental samples, while providing insight into mechanisms of persistence. Critically, we found that as death rates declined over time, lifespan was extended through the scavenging of dead cells. Although growth and reproduction were dramatically suppressed in the absence of an exogenous resource supply, bacterial populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of negative selection as well as molecular signals of adaptation. Remarkable consistency in the ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy-limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.

Coexisting species often exhibit negative frequency dependence due to mechanisms that promote population growth and persistence when rare. These stabilizing mechanisms maintain diversity through interspecific niche differences, but also through life-history strategies like dormancy that buffer dynamics in fluctuating environments. However, there are few tests demonstrating how seed banks contribute to long-term community dynamics and the maintenance of diversity. Using multi-year, high-frequency bacterial community data from a north temperate lake, we documented patterns consistent with stabilizing coexistence, including differential responses of bacterial taxa to environmental conditions and the presence of a seed bank. By maintaining rare taxa over winter periods, the seed bank contributed to recurrent seasonal dynamics. Last, strong negative frequency dependence in rare, but metabolically active, taxa suggested biotic interactions promoted coexistence. Together, our results provide field-based evidence that niche differences and seed banks stabilize bacterial community dynamics and contribute to the maintenance of microbial diversity in nature.

While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. Still, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant-soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. Then, in a factorially designed experiment, we applied the Rpf to soil containing field mustard (Brassica rapa), an agronomically important plant species. Plant biomass was ~33 % lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant-soil feedbacks in ways that affect above- and below-ground biodiversity and function.

The degree that the environment determines what genes contribute towards adaptation is a fundamental question in microbial evolution. Microbial populations are often experimentally passaged in different environments and sequenced in order to identify candidates for adaptation in a particular environment. However, there remains the need to develop an appropriate statistical framework to identify genes that acquired more mutations in one environment over the other (i.e., divergent evolution). Here we demonstrate how the evolutionary outcomes among replicate populations in the same environment, known as parallel evolution, can be leveraged to construct an intuitive statistical test for identifying the genes that contribute towards divergent evolution. To accomplish this task, we examined publicly available evolve-and-resequence experiment datasets and found that the distribution of mutation counts among genes can be predicted using an ensemble of independent Poisson random variables. Building on this result, we propose that the degree of divergent evolution at a given gene between populations from two different environments can be modeled as the difference between two Poisson random variables, known as the Skellam distribution. We then propose and apply a statistical test to identify specific genes that contribute towards divergent evolution. IMPORTANCE: There is currently no existing framework that can be leveraged to identify genes that contribute towards divergent evolution in microbial evolution experiments. To correct for this absence, we investigated the distribution of mutation counts among genes in order to identify an appropriate null model. Our observations suggest that divergent evolution within a given gene can be modeled as the difference in the total number of mutations observed between two environments. This quantity is described by a probability distribution known as the Skellam distribution, providing an appropriate statistical test for researchers seeking to identify the set of genes that contribute towards divergent evolution in evolution experiments.

Tidal freshwater marshes (TFMs) are threatened by seawater intrusion, which can affect microbial communities and alter biogeochemical processes. Here, we report on Seawater Addition Long Term Experiment (SALTEx), a manipulative field experiment that investigated continuous (press) and episodic (pulse, 2 months/yr) inputs of brackish water on microbial communities in a TFM. After 2.5 years, microbial diversity was lower in press treatments than in control (untreated) plots. Sulfate reducers increased in response to both press and pulse treatments whereas methanogens did not differ among treatments. Our results suggest that microbial communities in TFMs are resilient to episodic events, but that continuous seawater intrusion may alter bacterial diversity in ways that affect ecosystem functioning.Scientific Significance StatementSea level rise and seawater intrusion threaten tidal freshwater marshes (TFMs) and the important ecosystem services they provide. Intrusion of seawater in TFMs can occur across a range of timescales, such as episodic events, like storm surges or drought, or continuous intrusion as a result of rising sea level. The effects of these stressors on TFM microbial communities are not well understood. Our multi-year field manipulation of brackish water inputs revealed that microbial communities were resilient to short-term pulses of salinity whereas continuous seawater intrusion led to reduced microbial diversity along with changes in relative abundance of key functional groups. Such alterations may diminish the ability of TFMs to sequester carbon and cycle nutrients.

Much of Earth's biodiversity has the capacity to engage in dormancy, a reversible state of reduced metabolic activity. By increasing resilience to unfavourable conditions, dormancy leads to the accumulation of ‘seed banks’. These reservoirs of genetic and phenotypic diversity should diminish the strength of environmental filtering and increase rates of dispersal. Although prevalent among single-celled organisms, evidence that dormancy influences patterns of microbial biogeography is lacking. We constructed geographical and environmental distance–decay relationships (DDRs) for the total (DNA) and active (RNA) portions of bacterial communities in a regional-scale 16S rRNA survey of forested ponds in Indiana, USA. As predicted, total communities harboured greater diversity and exhibited weaker DDRs than active communities. These observations were robust to random resampling and different community metrics. To evaluate the processes underlying the biogeographic patterns, we developed a platform of mechanistic models that used the geographical coordinates and environmental characteristics of our study system. Based on more than 10 6 simulations, our models approximated the empirical DDRs when there was strong environmental filtering along with the presence of long-lived seed banks. By contrast, the inclusion of dispersal generally decreased model performance. Together, our findings support recent theoretical predictions that seed banks can influence the biogeographic patterns of microbial communities. This article is part of the theme issue ‘Conceptual challenges in microbial community ecology’.

A major goal of metacommunity ecology is to infer the local- and regional-scale processes that underlie community assembly. In dendritic ecological networks, branching patterns and directional flow can alter the balance between local and regional factors during assembly. Vertical habitat structure may further affect community assembly in dendritic metacommunities. In this study, we analyzed the bacterial metacommunity of a fifth-order mountain stream network to assess differences in community assembly (1) between planktonic and benthic habitats, (2) across spatial scales, and (3) between headwater and downstream regions of the network. Using taxonomic and phylogenetic null modeling, we found habitat-specific spatial patterns of community assembly across the dendritic network. Compositional differences between planktonic and benthic communities were maintained by variable selection, but we also found evidence of local dispersal limitation between the two habitats. Planktonic community assembly was scale dependent, transitioning from homogeneous selection at local scales to variable selection at regional scales, while benthic community assembly was less scale dependent. Variable selection structured headwaters in both habitat types, but downstream communities were primarily structured by homogeneous selection, especially in sediments. Taken together, our results show that vertical habitat structure contributes to the scale-dependent processes of community assembly across the dendritic metacommunity.

A major goal of metacommunity ecology is to infer the local- and regional-scale processes that underlie community assembly. In dendritic ecological networks (e.g., stream metacommunities), branching and directional dispersal connectivity can alter the balance between local and regional factors during assembly. However, the implications of vertical habitat structure (e.g., planktonic versus benthic sediments) in dendritic metacommunities remain unclear. In this study, we analyzed the bacterial metacommunity of a fifth-order mountain stream network to assess habitat differences in the (1) dominant community assembly processes, (2) spatial scaling of community assembly processes, and (3) longitudinal variation in community assembly. Using taxonomic and phylogenetic null modeling approaches, we found habitat-specific spatial patterns of community assembly across the dendritic network. Compositional differences between planktonic and benthic communities were maintained by divergent species sorting, but stochasticity influenced assembly at local scales. Planktonic communities showed scale-dependent assembly, transitioning from convergent sorting at local scales to divergent sorting at regional scales, while sediment community assembly was less scale dependent (convergent sorting remained important across all scales). While divergent sorting structured headwaters in both habitat types, sediment communities converged in structure downstream. Taken together, our results show that vertical habitat structure regulates the scale-dependent processes of community assembly across the dendritic metacommunity.

Until recently, our planet was thought to be home to ~10^7 species, largely belonging to plants and animals. Despite being the most abundant organisms on Earth, the contribution of microbial life to global biodiversity has been greatly underestimated and, in some cases, completely overlooked. Using a compilation of data known as the Global Prokaryotic Census (GPC), it was recently claimed that there are ~10^6 extant bacterial and archaeal taxa [1], an estimate that is orders of magnitude lower than predictions for global microbial biodiversity based on the lognormal model of biodiversity and diversity-abundance scaling laws [2]. Here, we resolve this discrepancy by 1) identifying violations of sampling theory, 2) correcting for the misuse of biodiversity theory, and 3) conducting a reanalysis of the GPC. By doing so, we uncovered greater support for diversity-abundance scaling laws and the lognormal model of biodiversity, which together predict that Earth is home to 10^12 or more microbial taxa.