The diversity and functional capacity of microbes associated with coastal macrophytes

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Miranda, K., Weigel, B., Fogarty, E., Veseli, I., Giblin, A., Eren, A., & Pfister, C. The diversity and functional capacity of microbes associated with coastal macrophytes. MSystems, 7(5),(2022): e0059222, https://doi.org/10.1128/msystems.00592-22.Coastal marine macrophytes 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 hosts through metabolisms that are unique to microbial taxa. Here, we characterized the metabolic functions of macrophyte-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.), the seagrass Zostera marina, and the sediments surrounding P. scouleri and Z. marina. Using metagenomic sequencing, we describe 63 metagenome-assembled genomes (MAGs) that potentially benefit from being associated with macrophytes and may contribute to macrophyte fitness through their metabolic activity. Host-associated metagenomes contained genes for the use of dissolved organic matter from hosts and vitamin (B1, B2, B7, B12) biosynthesis in addition to a range of nitrogen and sulfur metabolisms that recycle dissolved inorganic nutrients into forms 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 influences on carbon and nitrogen cycling in nearshore ecosystems.We thank The University of Chicago’s Microbiome Center for pilot award funding, Washington Department of Natural Resources, grants 93099282 and 93100399 (CAP), and NSF-DEB grant (no. 1556874) awarded to J.T. Wootton. We appreciate the work of C. Sauceda in the isotope analysis, as well as A. Wootton, A. Wood, and K. Foreman in the field sampling. S. Owens and S. Greenwald at Argonne National Lab provided expertise in sequencing. K.M. was supported by an EE Fellowship from The University of Chicago