The diversity and functional capacity of microbes associated with coastal phototrophs

Abstract

Coastal marine phototrophs exhibit some of the highest rates of primary productivity in the world. They have been found to host a diverse set of microbes, many of which may impact the biology of their phototroph hosts through metabolisms that are unique to microbial taxa. Here we characterized the metabolic functions of phototroph-associated microbial communities using metagenomes collected from 2 species of kelp (Laminaria setchellii and Nereocystis luetkeana) and 3 marine angiosperms (Phyllospadix scouleri, P. serrulatus and Zostera marina), including the rhizomes of two surfgrass species (Phyllospadix spp.) and the seagrass Zostera marina, and the sediments surrounding P. scouleri and Z. marina. Using metagenomic sequencing, we describe 72 metagenome assembled genomes (MAGs) that potentially benefit from being associated with macrophytes and may contribute to macrophyte fitness through their metabolic gene content. All host-associated metagenomes contained genes for the use of dissolved organic matter from hosts and vitamin (B1, B2, B7, B12) biosynthesis. Additionally, we found a range of nitrogen metabolism genes that transform dissolved inorganic nitrogen into forms that may be more available to the host. The rhizosphere of surfgrass and seagrass contained genes for anaerobic microbial metabolisms, including nifH genes associated with nitrogen fixation, despite residing in a well-mixed and oxygenated environment. The range of oxygen environments engineered by macrophytes likely explains the diversity of both oxidizing and reducing microbial metabolisms, and contributes to the functional capabilities of microbes and their influence on carbon and nitrogen cycling in nearshore ecosystems. ImportanceKelps, seagrasses and surfgrasses are ecosystem engineers on rocky shorelines where they show remarkably high levels of primary production. Through analysis of their associated microbial communities, we found a variety of microbial metabolisms that may benefit the host, including nitrogen metabolisms and the production of B vitamins. In turn, these microbes have the genetic capability to assimilate the dissolved organic compounds released by their phototroph hosts. We describe a range of oxygen environments associated with surfgrass, including low-oxygen microhabitats in their rhizomes that host genes for nitrogen fixation. The tremendous productivity of coastal phototrophs is likely due in part to the activities of associated microbes and an increased understanding of these associations is needed.