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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 (B 1 , B 2 , B 7 , B 12 ) 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.

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 B 12 ), 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 B 12 biosynthesis, and nitrogen reduction from nitrate and urea to ammonium, potentially providing the host kelp with vitamins and reduced nitrogen.

Background: Elucidating the spatial structure of host-associated microbial communities is essential for understanding taxon-taxon interactions within the microbiota and between microbiota and host. Macroalgae are colonized by complex microbial communities, suggesting intimate symbioses that likely play key roles in both macroalgal and bacterial biology, yet little is known about the spatial organization of microbes associated with macroalgae. Canopy-forming kelp are ecologically significant, fixing teragrams of carbon per year in coastal kelp forest ecosystems. We characterized the micron-scale spatial organization of bacterial communities on blades of the kelp Nereocystis luetkeana using fluorescence in situ hybridization and spectral imaging with a probe set combining phylum-, class-, and genus-level probes to localize and identify > 90% of the microbial community., Results: We show that kelp blades host a dense microbial biofilm composed of disparate microbial taxa in close contact with one another. The biofilm is spatially differentiated, with clustered cells of the dominant symbiont Granulosicoccus sp. (Gammaproteobacteria) close to the kelp surface and filamentous Bacteroidetes and Alphaproteobacteria relatively more abundant near the biofilm-seawater interface. A community rich in Bacteroidetes colonized the interior of kelp tissues. Microbial cell density increased markedly along the length of the kelp blade, from sparse microbial colonization of newly produced tissues at the meristematic base of the blade to an abundant microbial biofilm on older tissues at the blade tip. Kelp from a declining population hosted fewer microbial cells compared to kelp from a stable population., Conclusions: Imaging revealed close association, at micrometer scales, of different microbial taxa with one another and with the host. This spatial organization creates the conditions necessary for metabolic exchange among microbes and between host and microbiota, such as provisioning of organic carbon to the microbiota and impacts of microbial nitrogen metabolisms on host kelp. The biofilm coating the surface of the kelp blade is well-positioned to mediate interactions between the host and surrounding organisms and to modulate the chemistry of the surrounding water column. The high density of microbial cells on kelp blades (10 5 -10 7 cells/cm 2 ), combined with the immense surface area of kelp forests, indicates that biogeochemical functions of the kelp microbiome may play an important role in coastal ecosystems. Video abstract., (© 2022. The Author(s).)

We examined factors shaping community assembly of the bull kelp (Nereocystis luetkeana) microbiome by comparing microbial biofilm formation on photosynthetic kelp blade tissues and artificial kelp substrates ('agar substrates') deployed into a kelp forest. New kelp blade tissues were colonized by markedly distinct microbial taxa relative to agar substrates during the same time interval, even when agar substrates were infused with N. luetkeana blades, suggesting that microbial settlement onto kelp surfaces is more than just attraction to a polysaccharide-rich surface. Further, common seawater taxa such as Colwellia sp. and Psychromonas sp. became abundant on agar substrates but avoided new kelp blade tissues, indicating that host-specific factors may deter certain surface-associated marine microbial taxa. Over two-thirds of the bacterial taxa in the kelp microbiome were associated with strictly aerobic metabolisms; thus, photosynthetic production of O 2 may favour aerobic microbial metabolisms. While living kelp blades primarily recruited aerobic microbes, including the obligate aerobe Granulosicoccus sp., microbes that colonized agar substrates were predominantly facultative anaerobes. We also found that infusion of kelp tissues into agar substrates altered microbial community composition and lowered taxonomic diversity relative to control agar substrates, suggesting that non-living components of the kelp blade also impact microbial community assembly., (© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.)

Kelp forests are known as key habitats for species diversity and macroalgal productivity; however, we know little about how these biogenic habitats interact with seawater chemistry and phototroph productivity in the water column. We examined kelp forest functions at three locales along the Olympic Peninsula of Washington state by quantifying carbonate chemistry, nutrient concentrations, phytoplankton productivity, and seawater microbial communities inside and outside of kelp beds dominated by the canopy kelp species Nereocystis luetkeana and Macrocystis pyrifera. Kelp beds locally increased the pH, oxygen, and aragonite saturation state of the seawater, but lowered seawater inorganic carbon content and total alkalinity. Although kelp beds depleted nitrate and phosphorus concentrations, ammonium and dissolved organic carbon (DOC) concentrations were enhanced. Kelp beds also decreased chlorophyll concentrations and carbon fixed by phytoplankton, although kelp carbon fixation more than compensated for any difference in phytoplankton production. Kelp beds entrained distinct microbial communities, with higher taxonomic and phylogenetic diversity compared to seawater outside of the kelp bed. Kelp forests thus had significant effects on seawater chemistry, productivity and the microbial assemblages in their proximity. Thereby, the diversity of pathways for carbon and nitrogen cycling was also enhanced. Overall, these observations suggest that the contribution of kelp forests to nearshore carbon and nitrogen cycling is greater than previously documented., (© 2019 by the Ecological Society of America.)

Microbial symbionts in sponges are ubiquitous, forming complex and highly diverse host-specific communities. Conspecific sponges display remarkable stability in their symbiont communities, both spatially and temporally, yet extreme fluctuations in environmental factors can cause shifts in host-symbiont associations. We previously demonstrated that the marine sponge Hymeniacidon heliophila displayed significant community-level differences in microbial symbiont diversity, structure and composition when sampled from intertidal and subtidal environments. Here, we conducted a 70-day reciprocal transplant experiment to directly test the effect of tidal exposure on the microbiome of H. heliophila, using next-generation Illumina sequencing of 16S rRNA gene sequences to characterize symbiont communities. While sponges transplanted between habitats displayed shifts in microbial communities after 70 days, temporal variation was the dominant factor affecting microbial community composition. Further, we identified core symbionts that persisted across these spatio-temporal scales and used a metagenomic approach to show that these dominant members of the microbiome of H. heliophila represent nitrogen cycling taxa that have the potential to contribute to a diverse array of nitrogen transformations in the sponge holobiont. Together, these results indicate that despite moderate spatio-temporal shifts in symbiont composition, core symbiont functions (e.g. nitrogen cycling) can be maintained in sponge microbiomes through functional redundancy.