Compositional and Functional Microbiome Variation Between Tubes of an Intertidal Polychaete and Surrounding Marine Sediment

Abstract

The decorator worm Diopatra cuprea, a tube-forming marine polychaete common to intertidal and shallow subtidal waters, modifies habitats it occupies through microreef construction and algal gardening. While several studies have demonstrated that decorator worm tubes are hotspots of biogeochemical activity (i.e., nitrogen and sulfur cycling), it is still largely unclear whether the tube microbiome differs compositionally from the surrounding sediment and what distinct functional processes tube microbiomes may have. To address these unknowns, this study analyzed the bacterial communities of D. cuprea tubes and surrounding sediments using high-throughput 16S rRNA gene amplicon sequencing. Tubes and sediments were sampled at three sites along an anthropogenic stress gradient within the Newport River Estuary to also assess geographic variation of tube microbiomes and the possible influence of human disturbance. We found a clear distinction in the microbial community composition and diversity between tubes and surrounding sediment. Tube microbiomes were significantly enriched for the phyla Bacteriodetes, Actinobacteria, Verrucomicrobia, Deferribacteres, Latescibacteria, and Lentisphaerae. Chloroplast sequences of macroalgae and grass species were consistently abundant in tubes and nearly absent in surrounding sediment. Functional annotation of prokaryotic taxa (FAPROTAX)-based functional predictions suggested that tube microbiomes have higher potentials for aerobic chemoheterotrophy, sulfur compound respiration, nitrate reduction, methylotrophy, and hydrocarbon degradation than surrounding sediments. Tube microbiomes vary across sites, though dissimilarity is comparatively low compared to tube-to-sediment differences. Contrary to our hypothesis, the tubes at the most highly impacted site had the highest microbial diversity [i.e., amplicon sequence variant (ASV) richness and Shannon’s diversity], yet tubes from the medium impacted site actually had the lowest microbial diversity. Our findings show that D. cuprea tubes support a microbiome that is significantly distinct in composition and function from the surrounding sediment. Diopatra cuprea tubes appear to create unique microhabitats that facilitate numerous microbially-mediated biogeochemical processes in the marine benthic environment.

First screening of bacteria assemblages associated with the marine polychaete Melinna palmata Grube, 1870 and adjacent sediments

“…sediments (Liu et al, 2023). Thus, the tube-dwelling organisms often create microenvironments with particular conditions which might favor the colonization with specific bacterial communities (Fuirst et al, 2021). Moreover, sediments belong to a more heterogeneous and diverse set of microhabitats, creating a range of niches that can support a wider diversity of bacterial communities (Liu et al, 2023).…”

“…A high representation of Actionomarinales in Melinna tissue could be due to the adaptation of some of Actinobacteria taxa to colonize marine organisms such as sponges, molluscs, and polychaete tubes, constituting important sources for natural products with pharmaceutical applications (Konig et al, 2006;Fuirst et al, 2021). Meanwhile, the order Microtrichales of Actinobacteria showed a higher relative abundance within sediments.…”

Phoronids and their tubes harbor distinct microbiomes compared to surrounding sediment

“…[27]), have described important roles for the microbiome in hostenvironment interactions including metal resistance and sulfur cycling [28][29][30]. Often the microenvironment of the tube or burrow created by these marine organisms is found to have a distinct microbiome from surrounding sediments [22,23,28,31]. For example, blue mud shrimp burrows [27] introduce oxygen into local sediment which supports biogeochemical zonation around the burrow and may promote growth of sulfur cycling microbes.…”

Advances in Graduate Training in Integrative Bioinformatics for Investigating and Engineering Microbiomes (IBIEM)

“…These team research experiences were among the most highly rated training components and linked to gains across technical, communication, and collaboration skills. Example team research projects are listed below (related publications listed in reference section): Exploring the relationship between host phylogeny and gut microbiome structure across lemur species [14]; Impact of Copper Nanopesticides on Microbial Communities in Wetland and Terrestrial Ecosystems [15]; Effects of starvation and re-feeding on the microbiomes of the zebrafish intestine and environment [16]; and Microbiomes of oysters in oyster reefs and oysters in floating aquaculture [17].…”