Transitivity and intransitivity in soil bacterial networks.

Competition can lead to the exclusion of bacterial taxa when there is a transitive relationship among competitors with a hierarchy of competitive success. However, competition may not prevent bacterial coexistence if competitors form intransitive loops, in which none is able to outcompete all the rest. Both transitive and intransitive competition have been demonstrated in bacterial model systems. However, in natural soil microbial assemblages competition is typically understood as a dominance relationship leading to the exclusion of weak competitors. Here, we argue that transitive and intransitive interactions concurrently determine the structure of soil microbial communities. We explain why pairwise interactions cannot depict competition correctly in complex communities, and propose an alternative through the detection of strongly connected components (SCCs) in microbial networks. We finally analyse the existence of SCCs in soil bacterial communities in two Mediterranean ecosystems, for illustrative purposes only (rather than with the aim of providing a methodological tool) due to current limitations, and discuss future avenues to experimentally test the existence of SCCs in nature.

Incorporating phylogenetic metrics to microbial co-occurrence networks based on amplicon sequences to discern community assembly processes.

Co-occurrence network analysis based on amplicon sequences is increasingly used to study microbial communities. Patterns of co-existence or mutual exclusion between pairs of taxa are often interpreted as reflecting positive or negative biological interactions. However, other assembly processes can underlie these patterns, including species failure to reach distant areas (dispersal limitation) and tolerate local environmental conditions (habitat filtering). We provide a tool to quantify the relative contribution of community assembly processes to microbial co-occurrence patterns, which we applied to explore soil bacterial communities in two dry ecosystems. First, we sequenced a bacterial phylogenetic marker in soils collected across multiple plots. Second, we inferred co-occurrence networks to identify pairs of significantly associated taxa, either co-existing more (aggregated) or less often (segregated) than expected at random. Third, we assigned assembly processes to each pair: patterns explained based on spatial or environmental distance were ascribed to dispersal limitation (2%-4%) or habitat filtering (55%-77%), and the remaining to biological interactions. Finally, we calculated the phylogenetic distance between taxon pairs to test theoretical expectations on the linkages between phylogenetic patterns and assembly processes. Aggregated pairs were more closely related than segregated pairs. Furthermore, habitat-filtered aggregated pairs were closer relatives than those assigned to positive interactions, consistent with phylogenetic niche conservatism and cooperativism among distantly related taxa. Negative interactions resulted in equivocal phylogenetic signatures, probably because different competitive processes leave opposing signals. We show that microbial co-occurrence networks mainly reflect environmental tolerances and propose that incorporating measures of phylogenetic relatedness to networks might help elucidate ecologically meaningful patterns.

Successional trajectories of soil bacterial communities in mine tailings: The role of plant functional traits.

Plant species identity is assumed to be a major driver of belowground microbial diversity and composition. However, diagnosing which plant functional traits are responsible for shaping microbial communities remains elusive. Primary succession on barren metalliferous mining substrates was selected as the framework to study above-belowground interactions, and plant functional traits that lead the successional trajectories of soil bacterial communities were identified. The impact of the plant functional group (i.e. trees, shrubs, dwarf shrubs, perennial grasses), a trait integrating the life span and morphological structure, on the bacterial primary succession was monitored. Bacterial diversity and composition was estimated along plant size gradients including over 90 scattered patches ranging from seedlings to mature multispecific patches. Soil bacterial diversity was affected by heavy metals levels and increased towards higher resource availability underneath mature patches, with stress-tolerant heterotrophs and phototrophs being replaced by competitive heterotrophs. The plant functional group modulated these general patterns and shrubs had the greatest impact belowground by inducing the largest increase in soil fertility. Functional traits related to leaf decomposability and root architecture further determined the composition and structure of bacterial communities. These results underline the importance of plant functional traits in the assembly of soil bacterial communities, and can help guiding restoration of degraded lands.

Opposing phylogenetic diversity gradients of plant and soil bacterial communities.

Plants and soil microbes show parallel patterns of species-level diversity. Diverse plant communities release a wider range of organics that are consumed by more microbial species. We speculated, however, that diversity metrics accounting for the evolutionary distance across community members would reveal opposing patterns between plant and soil bacterial phylogenetic diversity. Plant phylogenetic diversity enhances plant productivity and thus expectedly soil fertility. This, in turn, might reduce bacterial phylogenetic diversity by favouring one (or a few) competitive bacterial clade. We collected topsoils in 15 semi-arid plant patches and adjacent low-cover areas configuring a plant phylodiversity gradient, pyrosequenced the 16S rRNA gene to identify bacterial taxa and analysed soil fertility parameters. Structural equation modelling showed positive effects of both plant richness and phylogenetic diversity on soil fertility. Fertility increased bacterial richness but reduced bacterial phylogenetic diversity. This might be attributed to the competitive dominance of a lineage based on its high relative fitness. This suggests biotic interactions as determinants of the soil bacterial community assembly, while emphasizing the need to use phylogeny-informed metrics to tease apart the processes underlying the patterns of diversity.

Climate change, phenology, and butterfly host plant utilization.

Knowledge of how species interactions are influenced by climate warming is paramount to understand current biodiversity changes. We review phenological changes of Swedish butterflies during the latest decades and explore potential climate effects on butterfly-host plant interactions using the Orange tip butterfly Anthocharis cardamines and its host plants as a model system. This butterfly has advanced its appearance dates substantially, and its mean flight date shows a positive correlation with latitude. We show that there is a large latitudinal variation in host use and that butterfly populations select plant individuals based on their flowering phenology. We conclude that A. cardamines is a phenological specialist but a host species generalist. This implies that thermal plasticity for spring development influences host utilization of the butterfly through effects on the phenological matching with its host plants. However, the host utilization strategy of A. cardamines appears to render it resilient to relatively large variation in climate.

Abiotic stress tolerance and competition-related traits underlie phylogenetic clustering in soil bacterial communities.

Soil bacteria typically coexist with close relatives generating widespread phylogenetic clustering. This has been ascribed to the abiotic filtering of organisms with shared ecological tolerances. Recent theoretical developments suggest that competition can also explain the phylogenetic similarity of coexisting organisms by excluding large low-competitive clades. We propose that combining the environmental patterns of traits associated with abiotic stress tolerances or competitive abilities with phylogeny and abundance data, can help discern between abiotic and biotic mechanisms underlying the coexistence of phylogenetically related bacteria. We applied this framework in a model system composed of interspersed habitats of highly contrasted productivity and comparatively dominated by biotic and abiotic processes, i.e. the plant patch-gap mosaic typical of drylands. We examined the distribution of 15 traits and 3290 bacterial taxa in 28 plots. Communities showed a marked functional response to the environment. Conserved traits related to environmental stress tolerance (e.g. desiccation, formation of resistant structures) were differentially selected in either habitat, while competition related traits (e.g. organic C consumption, formation of nutrient-scavenging structures) prevailed under high resource availability. Phylogenetic clustering was stronger in habitats dominated by biotic filtering, suggesting that competitive exclusion of large clades might underlie the ecological similarity of co-occurring soil bacteria.