The Diversity and Functional Capacity of Microbes Associated with Coastal Macrophytes.

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.

Functional Insights into the Kelp Microbiome from Metagenome-Assembled Genomes.

Eukaryotic organisms evolved in a microbial world and often have intimate associations with diverse bacterial groups. Kelp, brown macroalgae in the order Laminariales, play a vital role in coastal ecosystems, yet we know little about the functional role of the microbial symbionts that cover their photosynthetic surfaces. Here, we reconstructed 79 bacterial metagenome-assembled genomes (MAGs) from blades of the bull kelp, Nereocystis luetkeana, allowing us to determine their metabolic potential and functional roles. Despite the annual life history of bull kelp, nearly half of the bacterial MAGs were detected across multiple years. Diverse members of the kelp microbiome, spanning 6 bacterial phyla, contained genes for transporting and assimilating dissolved organic matter (DOM), which is secreted by kelp in large quantities and likely fuels the metabolism of these heterotrophic bacteria. Bacterial genomes also contained alginate lyase and biosynthesis genes, involved in polysaccharide degradation and biofilm formation, respectively. Kelp-associated bacterial genomes contained genes for dissimilatory nitrate reduction and urea hydrolysis, likely providing a reduced source of nitrogen to the host kelp. The genome of the most abundant member of the kelp microbiome and common macroalgal symbiont, Granulosicoccus, contained a full suite of genes for synthesizing cobalamin (vitamin B12), suggesting that kelp-associated bacteria have the potential to provide their host kelp with vitamins. Finally, kelp-associated Granulosicoccus contained genes that typify the aerobic anoxygenic phototrophic bacteria, including genes for bacteriochlorophyll synthesis and photosystem II reaction center proteins, making them the first known photoheterotrophic representatives of this genus. IMPORTANCE Kelp (brown algae in the order Laminariales) are foundational species that create essential habitat in temperate and arctic coastal marine ecosystems. These photosynthetic giants host millions of microbial taxa whose functions are relatively unknown, despite their potential importance for host-microbe interactions and nutrient cycling in kelp forest ecosystems. We reconstructed bacterial genomes from metagenomic samples collected from blades of the bull kelp, Nereocystis luetkeana, allowing us to determine the functional gene content of specific members of the kelp microbiome. These bacterial genomes spanned 6 phyla and 19 families and included common alga-associated microbial symbionts such as Granulosicoccus. Key functions encoded in kelp-associated bacterial genomes included dissolved organic matter assimilation, alginate metabolism, vitamin B12 biosynthesis, and nitrogen reduction from nitrate and urea to ammonium, potentially providing the host kelp with vitamins and reduced nitrogen.

Differential impacts of alternate primary producers on carbon cycling.

Disturbance impacts the spatial distribution of primary producers, which can have cascading effects on ecosystem function. The lower-intertidal zone on the rocky shores of the Pacific Northwest is one such place where wave energy creates a mosaic-like distribution between two assemblages: surfgrass (Phyllospadix scouleri) meadows and macroalgal forests dominated by kelp. We simulated wave disturbance by experimentally removing patches of surfgrass monocultures, resulting in a macroalgal assemblage with increased diversity, biomass, and net primary productivity in the following year. Although surfgrass had a higher C:N compared to macroalgal assemblages, macroalgal assemblages achieved a higher biomass, fixed carbon at a faster rate, and released more dissolved organic carbon (DOC) during photosynthesis. Thus, despite similar standing amounts of carbon, macroalgal assemblages have increased carbon turnover-from fixation to DOC release. Comparative photophysiology indicated that surfgrasses have a competitive advantage over other macrophytes at low light levels, allowing them to persist when disturbance is reduced. Unexpectedly, disturbance in this system increased the potential for carbon sequestration when surfgrass monocultures were replaced by diverse macroalgae.