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Plant microbiomes depend on environmental conditions, stochasticity, host species, and genotype identity. Eelgrass (Zostera marina)is a unique system for plant–microbe interactions as a marine angiosperm growing in a physiologically-challenging environment with anoxic sediment, periodic exposure to air at low tide, and fluctuations in water clarity and flow. We tested the influence of host origin versus environment on eelgrass microbiome composition by transplanting 768 plants among four sites within Bodega Harbor, CA. Over three months following transplantation, we sampled microbial communities monthly on leaves and roots and sequenced the V4–V5 region of the 16S rRNA gene to assess community composition. The main driver of leaf and root microbiome composition was destination site; more modest effects of host origin site did not last longer than one month. Community phylogenetic analyses suggested that environmental filtering structures these communities, but the strength and nature of this filtering varies among sites and over time and roots and leaves show opposing gradients in clustering along a temperature gradient. We demonstrate that local environmental differences create rapid shifts in associated microbial community composition with potential functional implications for rapid host acclimation under shifting environmental conditions.

 

ABSTRACT We develop a method to artificially select for rhizosphere microbiomes that confer salt tolerance to the model grass Brachypodium distachyon grown under sodium salt stress or aluminum salt stress. In a controlled greenhouse environment, we differentially propagated rhizosphere microbiomes between plants of a nonevolving, highly inbred plant population; therefore, only microbiomes evolved in our experiment, but the plants did not evolve in parallel. To maximize microbiome perpetuation when transplanting microbiomes between plants and, thus, maximize response to microbiome selection, we improved earlier methods by (i) controlling microbiome assembly when inoculating seeds at the beginning of each selection cycle; (ii) fractionating microbiomes before transfer between plants to harvest, perpetuate, and select on only bacterial and viral microbiome components; (iii) ramping of salt stress gradually from minor to extreme salt stress with each selection cycle to minimize the chance of overstressing plants; (iv) using two nonselection control treatments (e.g., nonselection microbial enrichment and null inoculation) that permit comparison to the improving fitness benefits that selected microbiomes impart on plants. Unlike previous methods, our selection protocol generated microbiomes that enhance plant fitness after only 1 to 3 rounds of microbiome selection. After nine rounds of microbiome selection, the effect of microbiomes selected to confer tolerance to aluminum salt stress was nonspecific (these artificially selected microbiomes equally ameliorate sodium and aluminum salt stresses), but the effect of microbiomes selected to confer tolerance to sodium salt stress was specific (these artificially selected microbiomes do not confer tolerance to aluminum salt stress). Plants with artificially selected microbiomes had 55 to 205% greater seed production than plants with unselected control microbiomes. IMPORTANCE We developed an experimental protocol that improves earlier methods of artificial selection on microbiomes and then tested the efficacy of our protocol to breed root-associated bacterial microbiomes that confer salt tolerance to a plant. Salt stress limits growth and seed production of crop plants, and artificially selected microbiomes conferring salt tolerance may ultimately help improve agricultural productivity. Unlike previous experiments of microbiome selection, our selection protocol generated microbiomes that enhance plant productivity after only 1 to 3 rounds of artificial selection on root-associated microbiomes, increasing seed production under extreme salt stress by 55 to 205% after nine rounds of microbiome selection. Although we artificially selected microbiomes under controlled greenhouse conditions that differ from outdoor conditions, increasing seed production by 55 to 205% under extreme salt stress is a remarkable enhancement of plant productivity compared to traditional plant breeding. We describe a series of additional experimental protocols that will advance insights into key parameters that determine efficacy and response to microbiome selection. 

Temperature increases due to climate change have affected the distribution and severity of diseases in natural systems, causing outbreaks that can destroy host populations. Host identity, diversity, and the associated microbiome can affect host responses to both infection and temperature, but little is known about how they could function as important mediators of disease in altered thermal environments. We conducted an 8‐week warming experiment to test the independent and interactive effects of warming, host genotypic identity, and host genotypic diversity on the prevalence and intensity of infections of seagrass (Zostera marina) by the wasting disease parasite (Labyrinthula zosterae). At elevated temperatures, we found that genotypically diverse host assemblages had reduced infection intensity, but not reduced prevalence, relative to less diverse assemblages. This dilution effect on parasite intensity was the result of both host composition effects as well as emergent properties of biodiversity. In contrast with the benefits of genotypic diversity under warming, diversity actually increased parasite intensity slightly in ambient temperatures. We found mixed support for the hypothesis that a growth–defense trade‐off contributed to elevated disease intensity under warming. Changes in the abundance (but not composition) of a few taxa in the host microbiome were correlated with genotype‐specific responses to wasting disease infections under warming, consistent with the emerging evidence linking changes in the host microbiome to the outcome of host–parasite interactions. This work emphasizes the context dependence of biodiversity–disease relationships and highlights the potential importance of interactions among biodiversity loss, climate change, and disease outbreaks in a key foundation species.

 

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass ( Zostera marina ) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.