The Diversity and Functional Capacity of Microbes Associated with Coastal Macrophytes

Abstract

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. IMPORTANCE Kelps, 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, sulfur oxidation, and the production of B vitamins. In turn, these microbes have the genetic capabilities to assimilate the dissolved organic compounds released by their macrophyte 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 seaweeds and seagrasses is likely due in part to the activities of associated microbes, and an increased understanding of these associations is needed.

Keywords: host-microbiome relationships; kelp; macrophytes; marine microbiology; oxygen; seagrass; surfgrass.

FIG 1

Boxplot comparing the dissolved oxygen concentrations of macrophyte tissue in the water column (blue) and in the sediment-rhizome environment (red) of P. scouleri (pairwise t-test: P < 0.001) and P. serrulatus (pairwise t-test: P < 0.001). Sampling dates are represented by different colors.

FIG 2

Stacked bar plots showing the relative abundances of 63 metagenome-assembled genomes (MAGs) across 7 environmental samples, including 30 high quality and 33 medium quality MAGs. Only 1 MAG (UBA7415 sp002470515, a Gammaproteobacteria) was found in the bulb of N. luetkeana and is not displayed here.

FIG 3

Boolean heatmap of microbial metabolisms in the MAGs reported in Fig. 2 and in Data Set S1, Sheet 2, across all hosts, grouped as those that might benefit the host (“hosts benefit”) and microbial metabolisms that might use host provisioned metabolites (“microbes benefit”). Each tick along the x-axis corresponds to a MAG. The N. luetkeana blade MAGs are from Weigel et al. (2022). The suite of genes for DOC Uptake (Compatible Solutes, Carboxylic Acids, Carbohydrate Pentoses, and General Carbohydrates) and Ammonification Hydrolases are shown as present if any of their genes are found in our MAGs. The presence or absence of metabolisms related to Nitrogen and Sulfur Metabolisms and Vitamin Synthesis are determined by the Network Algorithm for Metabolism Detection (NAMeD) (see supplemental code at https://github.com/kkmiranda/PNWMetagenomes/tree/main/NAMeD). The suite of genes and metabolic pathways used in this analysis can be found in Data Set S1, Sheet 3. A figure with a detailed x-axis is provided in Fig. S2.

FIG 4

A phylogenetic tree of the nifH genes found on the rhizomes of P. serrulatus (PSE, n = 1) and the rhizomes and surrounding sediment of Z. marina (ZMA, n = 3 and 5, respectively). Some nifH genes group into Cluster I, including a sulfur oxidizing taxon on the rhizome of Z. marina and other taxa in Campylobacterota, including Sulfurovum. Cluster III contains taxa associated with rhizomes, including Desulfobulbus mediterraneus on P. serrulatus and a Desulfobacterales associated with Z. marina rhizomes.A bootstrap support of >90% is indicated by an orange dot at a branch fork. A detailed figure with uncollapsed clades is available in Fig. S3.