Jennifer B. H. Martiny

Resistance, resilience, and redundancy in microbial communities

Although it is generally accepted that plant community composition is key for predicting rates of ecosystem processes in the face of global change, microbial community composition is often ignored in ecosystem modeling. To address this issue, we review recent experiments and assess whether microbial community composition is resistant, resilient, or functionally redundant in response to four different disturbances. We find that the composition of most microbial groups is sensitive and not immediately resilient to disturbance, regardless of taxonomic breadth of the group or the type of disturbance. Other studies demonstrate that changes in composition are often associated with changes in ecosystem process rates. Thus, changes in microbial communities due to disturbance may directly affect ecosystem processes. Based on these relationships, we propose a simple framework to incorporate microbial community composition into ecosystem process models. We conclude that this effort would benefit from more empirical data on the links among microbial phylogeny, physiological traits, and disturbance responses. These relationships will determine how readily microbial community composition can be used to predict the responses of ecosystem processes to global change.

Beyond biogeographic patterns: processes shaping the microbial landscape

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.

Fundamentals of microbial community resistance and resilience.

Microbial communities are at the heart of all ecosystems, and yet microbial community behavior in disturbed environments remains difficult to measure and predict. Understanding the drivers of microbial community stability, including resistance (insensitivity to disturbance) and resilience (the rate of recovery after disturbance) is important for predicting community response to disturbance. Here, we provide an overview of the concepts of stability that are relevant for microbial communities. First, we highlight insights from ecology that are useful for defining and measuring stability. To determine whether general disturbance responses exist for microbial communities, we next examine representative studies from the literature that investigated community responses to press (long-term) and pulse (short-term) disturbances in a variety of habitats. Then we discuss the biological features of individual microorganisms, of microbial populations, and of microbial communities that may govern overall community stability. We conclude with thoughts about the unique insights that systems perspectives – informed by meta-omics data – may provide about microbial community stability.

Drivers of bacterial β-diversity depend on spatial scale

The factors driving β-diversity (variation in community composition) yield insights into the maintenance of biodiversity on the planet. Here we tested whether the mechanisms that underlie bacterial β-diversity vary over centimeters to continental spatial scales by comparing the composition of ammonia-oxidizing bacteria communities in salt marsh sediments. As observed in studies of macroorganisms, the drivers of salt marsh bacterial β-diversity depend on spatial scale. In contrast to macroorganism studies, however, we found no evidence of evolutionary diversification of ammonia-oxidizing bacteria taxa at the continental scale, despite an overall relationship between geographic distance and community similarity. Our data are consistent with the idea that dispersal limitation at local scales can contribute to β-diversity, even though the 16S rRNA genes of the relatively common taxa are globally distributed. These results highlight the importance of considering multiple spatial scales for understanding microbial biogeography.

Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems.

Background Marine microbial communities have been essential contributors to global biomass, nutrient cycling, and biodiversity since the early history of Earth, but so far their community distribution patterns remain unknown in most marine ecosystems. Methodology/Principal Findings The synthesis of 9.6 million bacterial V6-rRNA amplicons for 509 samples that span the global oceans surface to the deep-sea floor shows that pelagic and benthic communities greatly differ, at all taxonomic levels, and share <10% bacterial types defined at 3% sequence similarity level. Surface and deep water, coastal and open ocean, and anoxic and oxic ecosystems host distinct communities that reflect productivity, land influences and other environmental constraints such as oxygen availability. The high variability of bacterial community composition specific to vent and coastal ecosystems reflects the heterogeneity and dynamic nature of these habitats. Both pelagic and benthic bacterial community distributions correlate with surface water productivity, reflecting the coupling between both realms by particle export. Also, differences in physical mixing may play a fundamental role in the distribution patterns of marine bacteria, as benthic communities showed a higher dissimilarity with increasing distance than pelagic communities. Conclusions/Significance This first synthesis of global bacterial distribution across different ecosystems of the Worlds oceans shows remarkable horizontal and vertical large-scale patterns in bacterial communities. This opens interesting perspectives for the definition of biogeographical biomes for bacteria of ocean waters and the seabed.

It's all relative: ranking the diversity of aquatic bacterial communities

The study of microbial diversity patterns is hampered by the enormous diversity of microbial communities and the lack of resources to sample them exhaustively. For many questions about richness and evenness, however, one only needs to know the relative order of diversity among samples rather than total diversity. We used 16S libraries from the Global Ocean Survey to investigate the ability of 10 diversity statistics (including rarefaction, non-parametric, parametric, curve extrapolation and diversity indices) to assess the relative diversity of six aquatic bacterial communities. Overall, we found that the statistics yielded remarkably similar rankings of the samples for a given sequence similarity cut-off. This correspondence, despite the different underlying assumptions of the statistics, suggests that diversity statistics are a useful tool for ranking samples of microbial diversity. In addition, sequence similarity cut-off influenced the diversity ranking of the samples, demonstrating that diversity statistics can also be used to detect differences in phylogenetic structure among microbial communities. Finally, a subsampling analysis suggests that further sequencing from these particular clone libraries would not have substantially changed the richness rankings of the samples.

Microbiomes in light of traits: A phylogenetic perspective.

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 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] 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.

Microbial abundance and composition influence litter decomposition response to environmental change

Rates of ecosystem processes such as decomposition are likely to change as a result of human impacts on the environment. In southern California, climate change and nitrogen (N) deposition in particular may alter biological communities and ecosystem processes. These drivers may affect decomposition directly, through changes in abiotic conditions, and indirectly through changes in plant and decomposer communities. To assess indirect effects on litter decomposition, we reciprocally transplanted microbial communities and plant litter among control and treatment plots (either drought or N addition) in a grassland ecosystem. We hypothesized that drought would reduce decomposition rates through moisture limitation of decomposers and reductions in plant litter quality before and during decomposition. In contrast, we predicted that N deposition would stimulate decomposition by relieving N limitation of decomposers and improving plant litter quality. We also hypothesized that adaptive mechanisms would allow microbes to decompose litter more effectively in their native plot and litter environments. Consistent with our first hypothesis, we found that drought treatment reduced litter mass loss from 20.9% to 15.3% after six months. There was a similar decline in mass loss of litter inoculated with microbes transplanted from the drought treatment, suggesting a legacy effect of drought driven by declines in microbial abundance and possible changes in microbial community composition. Bacterial cell densities were up to 86% lower in drought plots and at least 50% lower on litter derived from the drought treatment, whereas fungal hyphal lengths increased by 13-14% in the drought treatment. Nitrogen effects on decomposition rates and microbial abundances were weaker than drought effects, although N addition significantly altered initial plant litter chemistry and litter chemistry during decomposition. However, we did find support for microbial adaptation to N addition with N-derived microbes facilitating greater mass loss in N plots than in control plots. Our results show that environmental changes can affect rates of ecosystem processes directly through abiotic changes and indirectly through microbial abundances and communities. Therefore models of ecosystem response to global change may need to represent microbial biomass and community composition to make accurate predictions.

Rapid diversification of coevolving marine Synechococcus and a virus

Marine viruses impose a heavy mortality on their host bacteria, whereas at the same time the degree of viral resistance in marine bacteria appears to be high. Antagonistic coevolution—the reciprocal evolutionary change of interacting species—might reconcile these observations, if it leads to rapid and dynamic levels of viral resistance. Here we demonstrate the potential for extensive antagonistic coevolution between the ecologically important marine cyanobacterium Synechococcus and a lytic virus. In a 6-mo-long replicated chemostat experiment, Synechococcus sp. WH7803 and the virus (RIM8) underwent multiple coevolutionary cycles, leading to the rapid diversification of both host and virus. Over the course of the experiment, we detected between 4 and 13 newly evolved viral phenotypes (differing in host range) and between 4 and 11 newly evolved Synechococcus phenotypes (differing in viral resistance) in each chemostat. Genomic analysis of isolates identified several candidate genes in both the host and virus that might influence their interactions. Notably, none of the viral candidates were tail fiber genes, thought to be the primary determinants of host range in tailed bacteriophages, highlighting the difficulty in generalizing results from bacteriophage infecting γ-Proteobacteria. Finally, we show that pairwise virus–host coevolution may have broader community consequences; coevolution in the chemostat altered the sensitivity of Synechoccocus to a diverse suite of viruses, as well as the virus’ ability to infect additional Synechococcus strains. Our results indicate that rapid coevolution may contribute to the generation and maintenance of Synechococcus and virus diversity and thereby influence viral-mediated mortality of these key marine bacteria.

Is there a cost of virus resistance in marine cyanobacteria

Owing to their abundance and diversity, it is generally perceived that viruses are important for structuring microbial communities and regulating biogeochemical cycles. The ecological impact of viruses on microbial food webs, however, may be influenced by evolutionary processes, including the ability of bacteria to evolve resistance to viruses and the theoretical prediction that this resistance should be accompanied by a fitness cost. We conducted experiments using phylogenetically distinct strains of marine Synechococcus (Cyanobacteria) to test for a cost of resistance (COR) to viral isolates collected from Mount Hope Bay, Rhode Island. In addition, we examined whether fitness costs (1) increased proportionally with ‘total resistance’, the number of viruses for which a strain had evolved resistance, or (2) were determined more by ‘compositional resistance’, the identity of the viruses to which it evolved resistance. A COR was only found in half of our experiments, which may be attributed to compensatory mutations or the inability to detect a small COR. When detected, the COR resulted in a ∼20% reduction in relative fitness compared to ancestral strains. The COR was unaffected by total resistance, suggesting a pleiotropic fitness response. Under competitive conditions, however, the COR was dependent on compositional resistance, suggesting that fitness costs were associated with the identity of a few particular viruses. Our study provides the first evidence for a COR in marine bacteria, and suggests that Synechococcus production may be influenced by the composition of co-occurring viruses.