Genetic architecture of heritable leaf microbes.

Host-associated microbiomes are shaped by both their environment and host genetics, and often impact host performance. The scale of host genetic variation important to microbes is largely unknown yet fundamental to the community assembly of host-associated microbiomes, with implications for the eco-evolutionary dynamics of microbes and hosts. Using Ipomoea hederacea, ivyleaf morning glory, we generated matrilines differing in quantitative genetic variation and leaf shape, which is controlled by a single Mendelian locus. We then investigated the relative roles of Mendelian and quantitative genetic variation in structuring the leaf microbiome and how these two sources of genetic variation contributed to microbe heritability. We found that despite large effects of the environment, both Mendelian and quantitative genetic host variation contribute to microbe heritability and that the cumulative small effect genomic differences due to matriline explained as much or more microbial variation than a single large effect Mendelian locus. Furthermore, our results are the first to suggest that leaf shape itself contributes to variation in the abundances of some phyllosphere microbes.IMPORTANCEWe investigated how host genetic variation affects the assembly of Ipomoea hederacea's natural microbiome. We found that the genetic architecture of leaf-associated microbiomes involves both quantitative genetic variation and Mendelian traits, with similar contributions to microbe heritability. The existence of Mendelian and quantitative genetic variation for host-associated microbes means that plant evolution at the leaf shape locus or other quantitative genetic loci has the potential to shape microbial abundance and community composition.

Community interactions among microbes give rise to host-microbiome mutualisms in an aquatic plant.

Microbiomes often benefit plants, conferring resistance to pathogens, improving stress tolerance, or promoting plant growth. As potential plant mutualists, however, microbiomes are not a single organism but a community of species with complex interactions among microbial taxa and between microbes and their shared host. The nature of ecological interactions among microbes in the microbiome can have important consequences for the net effects of microbiomes on hosts. Here, we compared the effects of individual microbial strains and 10-strain synthetic communities on microbial productivity and host growth using the common duckweed Lemna minor and a synthetic, simplified version of its native microbiome. Except for Pseudomonas protegens, which was a mutualist when tested alone, all of the single strains we tested were commensals on hosts, benefiting from plant presence but not increasing host growth relative to uninoculated controls. However, 10-strain synthetic microbial communities increased both microbial productivity and duckweed growth more than the average single-strain inoculation and uninoculated controls, meaning that host-microbiome mutualisms can emerge from community interactions among microbes on hosts. The effects of community inoculation were sub-additive, suggesting at least some competition among microbes in the duckweed microbiome. We also investigated the relationship between L. minor fitness and that of its microbes, providing some of the first empirical estimates of broad fitness alignment between plants and members of their microbiomes; hosts grew faster with more productive microbes or microbiomes. IMPORTANCE: There is currently substantial interest in engineering synthetic microbiomes for health or agricultural applications. One key question is how multi-strain microbial communities differ from single microbial strains in their productivity and effects on hosts. We tested 20 single bacterial strains and 2 distinct 10-strain synthetic communities on plant hosts and found that 10-strain communities led to faster host growth and greater microbial productivity than the average, but not the best, single strain. Furthermore, the microbial strains or communities that achieved the greatest cell densities were also the most beneficial to their hosts, showing that both specific single strains and multi-strain synthetic communities can engage in high-quality mutualisms with their hosts. Our results suggest that ~5% of single strains, as well as multi-strain synthetic communities comprised largely of commensal microbes, can benefit hosts and result in effective host-microbe mutualisms.