Biogeography of macro- and micro-organisms in the deep sea is, in part, shaped by naturally occurring heterogeneous habitat features of geological and biological origin such as seeps, vents, seamounts, whale and wood-falls. Artificial features including shipwrecks and energy infrastructure shape the biogeographic patterns of macro-organisms; how they influence microorganisms is unclear. Shipwrecks may function as islands of biodiversity for microbiomes, creating a patchwork of habitats with influence radiating out into the seabed. Here we show microbiome richness and diversity increase as a function of proximity to the historic deep-sea shipwreck Anona in the Gulf of Mexico. Diversity and richness extinction plots provide evidence of an island effect on microbiomes. A halo of core taxa on the seabed was observed up to 200 m away from the wreck indicative of the transition zone from shipwreck habitat to the surrounding environment. Transition zones around natural habitat features are often small in area compared to what was observed at Anona indicating shipwrecks may exert a large sphere of influence on seabed microbiomes. Historic shipwrecks are abundant, isolated habitats with global distribution, providing a means to explore contemporary processes shaping biogeography on the seafloor. This work is a case study for how built environments impact microbial biodiversity and provides new information on how arrival of material to the seafloor shapes benthic microbiomes.

Exposure to oil from the Deepwater Horizon spill may have lasting impacts on preservation of historic shipwrecks in the Gulf of Mexico. Submerged steel structures, including shipwrecks, serve as artificial reefs and become hotspots of biodiversity in the deep sea. Marine biofilms on submerged structures support settlement of microand macro-biota and may enhance and protect against corrosion. Disruptions in the local environment, including oil spills, may impact the role that biofilms play in reef preservation. To determine how the Deepwater Horizon spill potentially impacted shipwreck biofilms and the functional roles of the biofilm microbiome, experiments containing carbon steels disks (CSDs) were placed at five historic shipwreck sites located within, and external to the benthic footprint of the Deepwater Horizon spill. The CSDs were incubated for 16 weeks to enable colonization by biofilm-forming microorganisms and to provide time for in situ corrosion to occur. Biofilms from the CSDs, as well as sediment and water microbiomes, were collected and analyzed by 16S rRNA amplicon gene sequencing to describe community composition and determine the source of taxa colonizing biofilms. Biofilm metagenomes were sequenced to compare differential gene abundances at spill-impacted and reference sites. Biofilms were dominated by Zeta-, Alpha-, Epsilon-, and Gamma-proteobacteria. Sequences affiliated with the Mariprofundus and Sulfurimonas genera were prolific, and Roseobacter, and Colwellia genera were also abundant. Analysis of 16S rRNA sequences from sediment, water, and biofilms revealed sediment to be the main known source of taxa to biofilms at impacted sites. Differential gene abundance analysis revealed the two-component response regulator CreC, a gene involved in environmental stress response, to be elevated at reference sites compared to impacted sites within the spill plume fallout area on the seafloor. Genes for chemotaxis, motility, and alcohol dehydrogenases were differentially abundant at reference vs. impacted sites. Metal loss on CSDs was elevated at sites within the spill fallout plume. Time series images reveal that metal loss at a heavily impacted site, the German Submarine U-166, has accelerated since the spill in 2010. This study provides evidence that spill residues on the seafloor may impact biofilm communities and the preservation of historic steel shipwrecks.

Historic shipwrecks function as habitats for benthic organisms by providing food, refuge, and structure. They also form islands of biodiversity on the seabed, shaping microbial ecology and ecosystem processes. This study examined two wooden deep-sea shipwrecks at 525 and 1800 m water depth and probed their influence on sediment microbiomes and geochemistry. Microbiomes were investigated with 16S rRNA gene amplicon sequencing along 60 m transects extending in four directions from the hulls of the shipwrecks. Distance from shipwrecks and sediment depth both shaped microbiome structure. Archaeal alpha diversity was significantly and positively correlated with proximity to the deeper shipwreck while bacterial diversity was not to either. Archaeal community structure differed at both sites; the deeper site had a higher proportion of Bathyarchaeia and Lokiarchaeia proximate to shipwreck compared to the shallow location. Major bacterial communities were consistent at both sites, however, at the deeper site had higher abundance of Bacteroidetes, Chloroflexi, Desulfofarculales, and Desulfobacteriales. Core microbiome and differential abundance analyses revealed unique taxa nearest the shipwrecks compared to the surrounding seabed including organoheterotrophs, and cellulolytic and sulfur cycling taxa. Sediment carbon content influenced microbiome structure near the shipwrecks (5-10 m). We show that shipwrecks have a distinct sediment microbiome and form unique habitat patches on seabed, resembling those surrounding organic falls. The shipwreck influence was more pronounced at the deeper site, further from terrestrial influences signaling shipwrecks may be a significant source of organic matter in far-shore oligotrophic settings.

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Marine biofilms are essential biological components that transform built structures into artificial reefs. Anthropogenic contaminants released into the marine environment, such as crude oil and chemical dispersant from an oil spill, may disrupt the diversity and function of these foundational biofilms. To investigate the response of marine biofilm microbiomes from distinct environments to contaminants and to address microbial functional response, biofilm metagenomes were analyzed from two short-term microcosms, one using surface seawater (SSW) and the other using deep seawater (DSW). Following exposure to crude oil, chemical dispersant, and dispersed oil, taxonomically distinct communities were observed between microcosms from different source water challenged with the same contaminants and higher Shannon diversity was observed in SSW metagenomes. Marinobacter, Colwellia, Marinomonas, and Pseudoalteromonas phylotypes contributed to driving community differences between SSW and DSW. SSW metagenomes were dominated by Rhodobacteraceae, known biofilm-formers, and DSW metagenomes had the highest abundance of Marinobacter, associated with hydrocarbon degradation and biofilm formation. Association of source water metadata with treatment groups revealed that control biofilms (no contaminant) harbor the highest percentage of significant KEGG orthologs (KOs). While 70% functional similarity was observed among all metagenomes from both experiments, functional differences between SSW and DSW metagenomes were driven primarily by membrane transport KOs, while functional similarities were attributed to translation and signaling and cellular process KOs. Oil and dispersant metagenomes were 90% similar to each other in their respective experiments, which provides evidence of functional redundancy in these microbiomes. When interrogating microbial functional redundancy, it is crucial to consider how composition and function evolve in tandem when assessing functional responses to changing environmental conditions within marine biofilms. This study may have implications for future oil spill mitigation strategies at the surface and at depth and also provides information about the microbiome functional responses of biofilms on steel structures in the marine built environment.