Integrating pH into the metabolic theory of ecology to predict bacterial diversity in soil.

Microorganisms play essential roles in soil ecosystem functioning and maintenance, but methods are currently lacking for quantitative assessments of the mechanisms underlying microbial diversity patterns observed across disparate systems and scales. Here we established a quantitative model to incorporate pH into metabolic theory to capture and explain some of the unexplained variation in the relationship between temperature and soil bacterial diversity. We then tested and validated our newly developed models across multiple scales of ecological organization. At the species level, we modeled the diversification rate of the model bacterium Pseudomonas fluorescens evolving under laboratory media gradients varying in temperature and pH. At the community level, we modeled patterns of bacterial communities in paddy soils across a continental scale, which included natural gradients of pH and temperature. Last, we further extended our model at a global scale by integrating a meta-analysis comprising 870 soils collected worldwide from a wide range of ecosystems. Our results were robust in consistently predicting the distributional patterns of bacterial diversity across soil temperature and pH gradients-with model variation explaining from 7 to 66% of the variation in bacterial diversity, depending on the scale and system complexity. Together, our study represents a nexus point for the integration of soil bacterial diversity and quantitative models with the potential to be used at distinct spatiotemporal scales. By mechanistically representing pH into metabolic theory, our study enhances our capacity to explain and predict the patterns of bacterial diversity and functioning under current or future climate change scenarios.

Ecology and Evolution of Plant Microbiomes.

Microorganisms colonizing plant surfaces and internal tissues provide a number of life-support functions for their host. Despite increasing recognition of the vast functional capabilities of the plant microbiome, our understanding of the ecology and evolution of the taxonomically hyperdiverse microbial communities is limited. Here, we review current knowledge of plant genotypic and phenotypic traits as well as allogenic and autogenic factors that shape microbiome composition and functions. We give specific emphasis to the impact of plant domestication on microbiome assembly and how insights into microbiomes of wild plant relatives and native habitats can contribute to reinstate or enrich for microorganisms with beneficial effects on plant growth, development, and health. Finally, we introduce new concepts and perspectives in plant microbiome research, in particular how community ecology theory can provide a mechanistic framework to unravel the interplay of distinct ecological processes-i.e., selection, dispersal, drift, diversification-that structure the plant microbiome.

Biotic and abiotic factors interplay in structuring the dynamics of microbial co-occurrence patterns in tropical mountainsides.

Ecological interactions are important for maintaining biodiversity and ecosystem functions. Particularly in stream biofilms, little is known about the distributional patterns of different taxonomic groups and their potential interactions along elevational gradients. Here, we investigated the bacterial and fungal community structures of stream biofilms across elevational gradients on Mount Kilimanjaro, and explored patterns of their distribution, diversity, community structures, and taxa co-occurrence. We found that fungal and bacterial richness were more convergent at higher elevations, while their community structures became significantly more divergent. Inferred network complexity and stability significantly decreased with increasing elevation for fungi, while an opposite trend was observed for bacteria. Further quantitative analyses showed that network structures of bacteria and fungi were more divergent as elevation increased. This pattern was strongly associated with shifts in abiotic factors, such as mean annual temperatures, water PO43--P, and stream width. By constructing bipartite networks, we showed the fungal-bacterial network to be less redundant, more clustering, and unstable with increasing elevation. Abiotic factors (e.g., temperatures and stream width) and microbial community properties (i.e., structure and composition) significantly explained the dynamic changes in fungal-bacterial network properties. Taken together, this study provides evidence for the interplay of biotic and abiotic factors structuring potential microbial interactions in stream biofilms along a mountainside elevational gradient.

Divergent impacts of fertilization regimes on below-ground prokaryotic and eukaryotic communities in the Tibetan Plateau.

Chemical nutrient amendment by human activities can lead to environmental impacts contributing to global biodiversity loss. However, the comprehensive understanding of how below- and above-ground biodiversity shifts under fertilization regimes in natural ecosystems remains elusive. Here, we conducted a seven-year field experiment (2011-2017) and examined the effects of different fertilization on plant biodiversity and soil belowground (prokaryotic and eukaryotic) communities in the alpine meadow of the Tibetan Plateau, based on data collected in 2017. Our results indicate that nitrogen addition promoted total plant biomass but reduced the plant species richness. Conversely, phosphorus enrichment did not promote plant biomass and exhibited an unimodal pattern with plant richness. In the belowground realm, distinct responses of soil prokaryotic and eukaryotic communities were observed under fertilizer application. Specifically, soil prokaryotic diversity decreased with nitrogen enrichment, correlating with shifts in soil pH. Similarly, soil eukaryotic diversity decreased with increased phosphorous inputs, aligning with the equilibrium between soil available and total phosphorus. We also established connections between these soil organism communities with above-ground plant richness and biomass. Overall, our study contributes to a better understanding of the sustainable impacts of human-induced nutrient enrichment on the natural environment. Future research should delve deeper into the long-term effects of fertilization on soil health and ecosystem functioning, aiming to achieve a balance between agricultural productivity and environmental conservation.

Biogeographical patterns of abundant and rare bacterial biospheres in paddy soils across East Asia.

Soil bacterial communities play fundamental roles in ecosystem functioning and often display a skewed distribution of abundant and rare taxa. So far, relatively little is known about the biogeographical patterns and mechanisms structuring the assembly of abundant and rare biospheres of soil bacterial communities. Here, we studied the geographical distribution of different bacterial sub-communities by examining the relative influence of environmental selection and dispersal limitation on taxa distributions in paddy soils across East Asia. Our results indicated that the geographical patterns of four different bacterial sub-communities consistently displayed significant distance-decay relationships (DDRs). In addition, we found niche breadth and dispersal rates to significantly explain differences in community assembly of abundant and rare taxa, directly affecting the strength of DDRs. While conditionally rare and abundant taxa displayed the strongest DDR due to higher environmental filtering and dispersal limitation, moderate taxa sub-communities had the weakest DDR due to greater environmental tolerance and dispersal rate. Random forest models indicated that soil pH (9.13%-49.78%) and average annual air temperature (16.59%-46.49%) were the most important predictors of the variation in the bacterial community. This study advances our understanding of the intrinsic links between fundamental ecological processes and microbial biogeographical patterns in paddy soils.

Microbial phylogenetic relatedness links to distinct successional patterns of bacterial and fungal communities.

The mechanisms underlying microbial community dynamics and co-occurrence patterns along ecological succession are crucial for understanding ecosystem recovery but remain largely unexplored. Here, we investigated community dynamics and taxa co-occurrence patterns in bacterial and fungal communities across a well-established chronosequence of post-mining lands spanning 54 years of recovery. Bacterial community structures became increasingly phylogenetically clustered with soil age at early successional stages and varied less at later successional stages. The dynamics of bacterial community phylogenetic structures were determined by the changes in the soil vegetation cover along succession. The dynamics of fungal community phylogenetic structures did not significantly correlate with soil age, soil properties or vegetation cover, and were mainly attributed to stochastic processes. Along succession, the common decrease in the bacterial co-occurrence complexity and in the average pairwise phylogenetic distances between co-occurring bacteria implied a decrease in potential bacterial cooperation. The increased complexity of fungal co-occurrence along succession was independent of phylogenetic relatedness between co-occurring fungi. This study provides new sights into ecological mechanisms underlying bacterial and fungal community succession.

Soil Microbial Diversity Affects the Plant-Root Colonization by Arbuscular Mycorrhizal Fungi.

Terrestrial plants establish symbiosis with arbuscular mycorrhizal fungi (AMF) to exchange water and nutrients. However, the extent to which soil biodiversity influences such association remains still unclear. Here, we manipulated the soil microbial diversity using a "dilution-to-extinction" approach in a controlled pot microcosm system and quantified the root length colonization of maize plants by the AMF Rhizophagus clarus. The experiment was performed by manipulating the soil microbiome within a native and foreign soil having distinct physicochemical properties. Overall, our data revealed significant positive correlations between the soil microbial diversity and AMF colonization. Most importantly, this finding opposes the diversity-invasibility hypothesis and highlights for a potential overall helper effect of the soil biodiversity on plant-AMF symbiosis.

Divergent Co-occurrence Patterns and Assembly Processes Structure the Abundant and Rare Bacterial Communities in a Salt Marsh Ecosystem.

Understanding how species interaction and assembly processes structure the abundant and rare bacterial biospheres in soils is crucial for predicting how biodiversity influences ecosystem functioning. Here, we profiled the bacterial communities across a salt marsh ecosystem gradient to investigate the co-occurrence patterns across taxa and the relative influence of ecological processes mediating the assembly of the abundant and rare biospheres in soil. Our results revealed abundant taxa to be ubiquitous across all sites, whereas the distributions of the rare taxa were relatively more site specific. The α-diversity indices and ß-diversity of rare subcommunities were significantly higher than those of the abundant subcommunities. Besides, both the taxonomic and functional composition of soil bacterial communities differed significantly between the two biospheres. Furthermore, the influence of stochasticity differed in each subcommunity. In particular, stochastic processes were relatively more important in constraining the assembly of rare taxa. Co-occurrence network analysis revealed that a few abundant taxa occupy central nodes within the networks, possibly indicating crucial roles as keystone taxa. Collectively, these findings suggest that abundant and rare bacterial biospheres have distinct distributions underpinned by a dynamic interplay of ecological processes and taxon co-occurrence patterns.IMPORTANCE Estuarine salt marshes are highly productive ecosystems subjected to regular disturbances by hydrodynamic exchange. However, little is known about how distinct assembly processes and co-occurrence of taxa influence the structure of the abundant and rare bacterial biospheres in these soil systems. This study aims at unravelling these intricacies by studying a typical estuarine salt marsh located in Hangzhou Bay, China. Our study provides important pieces of evidence on the diverse distribution of rare and abundant bacterial biospheres. We show that a few abundant taxa are central nodes in species co-occurrence, potentially playing important roles as keystone species in the system. In addition, we highlight a dynamic interplay of assembly processes structuring these two subcommunities.

Dispersal mitigates bacterial dominance over microalgal competitor in metacommunities.

Ecological theory suggests that a combination of local and regional factors regulate biodiversity and community functioning in metacommunities. The relative importance of different factors structuring communities likely changes over successional time, but to date this concept is scarcely documented. In addition, the few studies describing successional dynamics in metacommunity regulation have only focused on a single group of organisms. Here, we report results of an experimental study testing the effect size of initial local community composition and dispersal between local patches on community dynamics of benthic microalgae and their associated bacteria over community succession. Our results show that over time dispersal outweighed initial effects of community composition on microalgal evenness and biomass, microalgal ß-diversity, and the ratio of bacteria to microalgae. At the end of the experiment (ca. 20 microalgae generations), dispersal significantly decreased microalgal evenness and ß-diversity by promoting one regionally superior competitor. Dispersal also decreased the ratio of bacteria to microalgae, while it significantly increased microalgal biomass. These results suggest that the dispersal-mediated establishment of a dominant and superior microalgae species prevented bacteria from gaining competitive advantage over the autotrophs in these metacommunities, ultimately maintaining the provision of autotrophic biomass. Our study emphasizes the importance of time for dispersal to be a relevant community-structuring mechanism. Moreover, we highlight the need for considering multiple competitors in complex metacommunity systems to properly pinpoint the consequences of local change in dominance through dispersal for metacommunity function.

Bacterial Community Assembly in a Typical Estuarine Marsh with Multiple Environmental Gradients.

Bacterial communities play essential roles in estuarine marsh ecosystems, but the interplay of ecological processes underlying their community assembly is poorly understood. Here, we studied the sediment bacterial communities along a linear gradient extending from the water-land junction toward a high marsh, using 16S rRNA gene amplicon sequencing. Bacterial community compositions differed significantly between sediment transects. Physicochemical properties, particularly sediment nutrient levels (i.e., total nitrogen [TN] and available phosphorus [AP]), as well as sediment physical structure and pH (P < 0.05), were strongly associated with the overall community variations. In addition, the topological properties of bacterial cooccurrence networks varied with distance to the water-land junction. Both node- and network-level topological features revealed that the bacterial network of sediments farthest from the junction was less intense in complexity and interactions than other sediments. Phylogenetic null modeling analysis showed a progressive transition from stochastic to deterministic community assembly for the water-land junction sites toward the emerging terrestrial system. Taken together, data from this study provide a detailed outline of the distribution pattern of the sediment bacterial community across an estuarine marsh and inform the mechanisms and processes mediating bacterial community assembly in marsh soils.IMPORTANCE Salt marshes represent highly dynamic ecosystems where the atmosphere, continents, and the ocean interact. The bacterial distribution in this ecosystem is of great ecological concern, as it provides essential functions acting on ecosystem services. However, ecological processes mediating bacterial assembly are poorly understood for salt marshes, especially the ones located in estuaries. In this study, the distribution and assembly of bacterial communities in an estuarine marsh located in south Hangzhou Bay were investigated. The results revealed an intricate interplay between stochastic and deterministic processes mediating the assembly of bacterial communities in the studied gradient system. Collectively, our findings illustrate the main drivers of community assembly, taking into consideration changes in sediment abiotic variables and potential biotic interactions. Thus, we offer new insights into estuarine bacterial communities and illustrate the interplay of ecological processes shaping the assembly of bacterial communities in estuarine marsh ecosystems.

Genomic signatures and co-occurrence patterns of the ultra-small Saccharimonadia (phylum CPR/Patescibacteria) suggest a symbiotic lifestyle.

The size of bacterial genomes is often associated with organismal metabolic capabilities determining ecological breadth and lifestyle. The recently proposed Candidate Phyla Radiation (CPR)/Patescibacteria encompasses mostly unculturable bacterial taxa with relatively small genome sizes with potential for co-metabolism interdependencies. As yet, little is known about the ecology and evolution of CPR, particularly with respect to how they might interact with other taxa. Here, we reconstructed two novel genomes (namely, Candidatus Saccharibacter sossegus and Candidatus Chaer renensis) of taxa belonging to the class Saccharimonadia within the CPR/Patescibacteria using metagenomes obtained from acid mine drainage (AMD). By testing the hypothesis of genome streamlining or symbiotic lifestyle, our results revealed clear signatures of gene losses in these genomes, such as those associated with de novo biosynthesis of essential amino acids, nucleotides, fatty acids and cofactors. In addition, co-occurrence analysis provided evidence supporting potential symbioses of these organisms with Hydrotalea sp. in the AMD system. Together, our findings provide a better understanding of the ecology and evolution of CPR/Patescibacteria and highlight the importance of genome reconstruction for studying metabolic interdependencies between unculturable Saccharimonadia representatives.

Compositional and abundance changes of nitrogen-cycling genes in plant-root microbiomes along a salt marsh chronosequence.

Disentangling the relative influences of soil properties and plant-host on root-associated microbiomes in natural systems is challenging, given that spatially segregated soil types display distinct historical legacies. In addition, distant locations may also lead to biogeographical patterns of microbial communities. Here, we used an undisturbed salt marsh chronosequence spanning over a century of ecosystem development to investigate changes in the community composition and abundance of a set of nitrogen-cycling genes. Specifically, we targeted genes of diazotrophs and ammonia oxidizers associated with the bulk and rhizosphere soil of the plant species Limonium vulgare. Samples were collected across five distinct successional stages of the chronosequence (ranging from 5 to 105 years) at two time-points. Our results indicate that soil variables such as sand:silt:clay % content and pH strongly relates to the abundance of N-cycling genes in the bulk soil. However, in the rhizosphere samples, the abundance of ammonia-oxidizing organisms (both bacteria and archaea, AOB and AOA, respectively) was relatively constant across most of the successional stages, albeit displaying seasonal variation. This result indicates a potentially stronger control of plant host (rather than soil) on the abundance of these organisms. Interestingly, the plant host did not have a significant effect on the composition of AOA and AOB communities, being mostly divergent according to soil successional stages. The abundance of diazotrophic communities in rhizosphere samples was more affected by seasonality than those of bulk soil. Moreover, the abundance pattern of diazotrophs in the rhizosphere related to the systematic increase of plant biomass and soil organic matter along the successional gradient. These results suggest a potential season-dependent regulation of diazotrophs exerted by the plant host. Overall, this study contributes to a better understanding of how the natural formation of a soil and host plants influence the compositional and abundance changes of nitrogen-cycling genes in bulk and rhizosphere soil microhabitats.

Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession.

Ecological succession and the balance between stochastic and deterministic processes are two major themes within microbial ecology, but these conceptual domains have mostly developed independent of each other. Here we provide a framework that integrates shifts in community assembly processes with microbial primary succession to better understand mechanisms governing the stochastic/deterministic balance. Synthesizing previous work, we devised a conceptual model that links ecosystem development to alternative hypotheses related to shifts in ecological assembly processes. Conceptual model hypotheses were tested by coupling spatiotemporal data on soil bacterial communities with environmental conditions in a salt marsh chronosequence spanning 105 years of succession. Analyses within successional stages showed community composition to be initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with increasing sodium concentration. Analyses of community turnover among successional stages--which provide a larger spatiotemporal scale relative to within stage analyses--revealed that changes in the concentration of soil organic matter were the main predictor of the type and relative influence of determinism. Taken together, these results suggest scale-dependency in the mechanisms underlying selection. To better understand mechanisms governing these patterns, we developed an ecological simulation model that revealed how changes in selective environments cause shifts in the stochastic/deterministic balance. Finally, we propose an extended--and experimentally testable--conceptual model integrating ecological assembly processes with primary and secondary succession. This framework provides a priori hypotheses for future experiments, thereby facilitating a systematic approach to understand assembly and succession in microbial communities across ecosystems.

Transcriptional Responses of the Bacterium Burkholderia terrae BS001 to the Fungal Host Lyophyllum sp. Strain Karsten under Soil-Mimicking Conditions.

In this study, the mycosphere isolate Burkholderia terrae BS001 was confronted with the soil fungus Lyophyllum sp. strain Karsten on soil extract agar plates in order to examine its transcriptional responses over time. At the initial stages of the experiment (T1-day 3; T2-day 5), contact between both partner organisms was absent, whereas in the final stage (T3-day 8), the two populations made intimate physical contact. Overall, a strong modulation of the strain BS001 gene expression patterns was found. First, the stationary-phase sigma factor RpoS, and numerous genes under its control, were strongly expressed as a response to the soil extract agar, and this extended over the whole temporal regime. In the system, B. terrae BS001 apparently perceived the presence of the fungal hyphae already at the early experimental stages (T1, T2), by strongly upregulating a suite of chemotaxis and flagellar motility genes. With respect to specific metabolism and energy generation, a picture of differential involvement in different metabolic routes was obtained. Initial (T1, T2) up- or downregulation of ethanolamine and mandelate uptake and utilization pathways was substituted by a strong investment, in the presence of the fungus, in the expression of putative metabolic gene clusters (T3). Specifically at T3, five clustered genes that are potentially involved in energy generation coupled to an oxidative stress response, and two genes encoding short-chain dehydrogenases/oxidoreductases (SDR), were highly upregulated. In contrast, the dnaE2 gene (related to general stress response; encoding error-prone DNA polymerase) was transcriptionally downregulated at this stage. This study revealed that B. terrae BS001, from a stress-induced state, resulting from the soil extract agar milieu, responds positively to fungal hyphae that encroach upon it, in a temporally dynamic manner. The response is characterized by phases in which the modulation of (1) chemotaxis, (2) metabolic activity, and (3) oxidative stress responses are key mechanisms.

Genes related to antioxidant metabolism are involved in Methylobacterium mesophilicum-soybean interaction.

The genus Methylobacterium is composed of pink-pigmented methylotrophic bacterial species that are widespread in natural environments, such as soils, stream water and plants. When in association with plants, this genus colonizes the host plant epiphytically and/or endophytically. This association is known to promote plant growth, induce plant systemic resistance and inhibit plant infection by phytopathogens. In the present study, we focused on evaluating the colonization of soybean seedling-roots by Methylobacterium mesophilicum strain SR1.6/6. We focused on the identification of the key genes involved in the initial step of soybean colonization by methylotrophic bacteria, which includes the plant exudate recognition and adaptation by planktonic bacteria. Visualization by scanning electron microscopy revealed that M. mesophilicum SR1.6/6 colonizes soybean roots surface effectively at 48 h after inoculation, suggesting a mechanism for root recognition and adaptation before this period. The colonization proceeds by the development of a mature biofilm on roots at 96 h after inoculation. Transcriptomic analysis of the planktonic bacteria (with plant) revealed the expression of several genes involved in membrane transport, thus confirming an initial metabolic activation of bacterial responses when in the presence of plant root exudates. Moreover, antioxidant genes were mostly expressed during the interaction with the plant exudates. Further evaluation of stress- and methylotrophic-related genes expression by qPCR showed that glutathione peroxidase and glutathione synthetase genes were up-regulated during the Methylobacterium-soybean interaction. These findings support that glutathione (GSH) is potentially a key molecule involved in cellular detoxification during plant root colonization. In addition to methylotrophic metabolism, antioxidant genes, mainly glutathione-related genes, play a key role during soybean exudate recognition and adaptation, the first step in bacterial colonization.

Engineering microbiomes to transform plastics.

The design and study of active microbial consortia able to degrade plastics represent an exciting area of research toward the development of bio-based alternatives to efficiently transform plastic waste. This forum article discusses concepts and mechanisms to inform emerging strategies for engineering microbiomes to transform plastics under controlled settings.

Toward an integrative framework for microbial community coalescence.

Community coalescence is defined as the mixing of intact ecological communities. From river confluences to fecal microbiota transplantation, community coalescence constitutes a common ecological occurrence affecting natural and engineered microbial systems. In this opinion article, we propose an integrative framework for microbial community coalescence to guide advances in our understanding of this important - yet underexplored - ecological phenomenon. We start by aligning community coalescence with the unified framework of biological invasion and enumerate commonalities and idiosyncrasies between these two analogous processes. Then, we discuss how organismal interactions and cohesive establishment affect coalescence outcomes with direct implications for community functioning. Last, we propose the use of ecological null modeling to study the interplay of ecological processes structuring community reassembly following coalescence.

Exploiting microbial competition to promote plant health.

The host-associated microbiota can promote colonization resistance against pathogens via a mechanism termed 'nutrient blocking', as highlighted in a recent article by Spragge et al. This implies that greater metabolic overlap between commensal taxa and pathogens leads to disease suppression. Here, we discuss future avenues for how this principle can be exploited in the rhizosphere microbiota to promote plant health.