The field of microbiome research is arguably one of the fastest growing in biology. Bacteria feature prominently in studies on animal health, but fungi appear to be the more prominent functional symbionts for plants. Despite the similarities in the ecological organization and evolutionary importance of animal-bacterial and plant–fungal microbiomes, there is a general failure across disciplines to integrate the advances made in each system. Researchers studying bacterial symbionts in animals benefit from greater access to efficient sequencing pipelines and taxonomic reference databases, perhaps due to high medical and veterinary interest. However, researchers studying plant–fungal symbionts benefit from the relative tractability of fungi under laboratory conditions and ease of cultivation. Thus each system has strengths to offer, but both suffer from the lack of a common conceptual framework. We argue that community ecology best illuminates complex species interactions across space and time. In this synthesis we compare and contrast the animal-bacterial and plant–fungal microbiomes using six core theories in community ecology (i.e., succession, community assembly, metacommunities, multi-trophic interactions, disturbance, restoration). The examples and questions raised are meant to spark discussion amongst biologists and lead to the integration of these two systems, as well as more informative, manipulatory experiments on microbiomes research.

Over the past 25 years, the plant-soil feedback (PSF) framework has catalyzed our understanding of how belowground microbiota impact plant fitness and species coexistence. Here, we apply a novel extension of this framework to microbiota associated with aboveground tissues, termed 'plant-phyllosphere feedback (PPFs)'. In parallel greenhouse experiments, rhizosphere and phyllosphere microbiota of con- and heterospecific hosts from four species were independently manipulated. In a third experiment, we tested the combined effects of soil and phyllosphere feedback under field conditions. We found that three of four species experienced weak negative PSF whereas, in contrast, all four species experienced strong negative PPFs. Field-based feedback estimates were highly negative for all four species, though variable in magnitude. Our results suggest that phyllosphere microbiota, like rhizosphere microbiota, can potentially mediate plant species coexistence via negative feedbacks. Extension of the PSF framework to the phyllosphere is needed to more fully elucidate plant-microbiota interactions.

Experimental tests of community assembly mechanisms for host-associated microbiomes in nature are lacking. Asymptomatic foliar fungal endophytes are a major component of the plant microbiome and are increasingly recognized for their impacts on plant performance, including pathogen defense, hormonal manipulation, and drought tolerance. However, it remains unclear whether fungal endophytes preferentially colonize certain host ecotypes or genotypes, reflecting some degree of biotic adaptation in the symbioses, or whether colonization is simply a function of spore type and abundance within the local environment. Whether host ecotype, local environment, or some combination of both controls the pattern of microbiome formation across hosts represents a new dimension to the age-old debate of nature versus nurture. Here we used a reciprocal transplant design to explore the extent of host specificity and biotic adaptation in the plant microbiome, as evidenced by differential colonization of host genetic types by endophytes. Specifically, replicate plants from three locally-adapted ecotypes of the native grass Panicum virgatum (switchgrass) were transplanted at three geographically distinct field sites (one home and two away) in the Midwestern US. At the end of the growing season, plant leaves were harvested and the fungal microbiome characterized using culture-dependent sequencing techniques. Our results demonstrated that fungal endophyte community structure was determined by local environment (i.e., site), but not by host ecotype. Fungal richness and diversity also strongly differed by site, with lower fungal diversity at a riparian field site, whereas host ecotype had no effect. By contrast, there were significant differences in plant phenotypes across all ecotypes and sites, indicating ecotypic differentiation of host phenotype. Overall, our results indicate that environmental factors are the primary drivers of community structure in the switchgrass fungal microbiome.

SummaryNutrient limitation is a basic ecological constraint that has received little attention in studies on virus production and disease dynamics. Nutrient availability could directly limit the production of viral nucleic acids and proteins, or alternatively limit host growth and thus indirectly limit metabolic pathways necessary for viral replication.In order to compare direct and indirect effects of nutrient limitation on virus production within hosts, we manipulated soil nitrogen (N) and phosphorus (P) availability in a glasshouse for the wild grass host Bromus hordeaceus and the viral pathogen Barley yellow dwarf virus-PAV.We found that soil N additions increased viral concentrations within host tissues, and the effect was mediated by host growth. Specifically, in statistical models evaluating the roles of host biomass production, leaf N and leaf P, viral production depended most strongly on host biomass, rather than the concentration of either nutrient. Furthermore, at low soil N, larger plants supported greater viral concentrations than smaller ones, whereas at high N, smaller plants supported greater viral concentrations.Our results suggest that enhanced viral productivity under N enrichment is an indirect consequence of nutrient stimulation to host growth rate. Heightened pathogen production in plants has important implications for a world facing increasing rates of nutrient deposition.