The densities of chemoautotrophic and methanotrophic symbiont morphotypes were determined in life- history stages (post-larvae, juveniles, adults) of two species of mussels (Bathymodiolus azoricus and B. heckerae) from deep-sea chemosynthetic environments (the Lucky Strike hydrothermal vent and the Blake Ridge cold seep) in the Atlantic Ocean. Both symbiont morphotypes were observed in all specimens and in the same relative proportions, regardless of life-history stage. The relative abundance of symbiont morphotypes, determined by transmission electron microscopy, was different in the two species: chemoautotrophs were dominant (13:1-18:1) in B. azoricus from the vent site; methanotrophs were dominant (2:1-3:1) in B. heckerae from the seep site. The ratio of CH4:H2S is proposed as a determinant of the relative abundance of symbiont types: where CH4:H2S is less than 1, as at the Lucky Strike site, chemoautotrophic symbionts dominate; where CH4:H2S is greater than 2, as at the seep site, methanotrophs dominate. Organic carbon and nitrogen isotopic compositions of B. azoricus (delta 13C = -30 per thousand; delta 15N = -9 per thousand) and B. heckerae (delta 13C = -56 per thousand; delta 15N = -2 per thousand) varied little among life-history stages and provided no record of a larval diet of photosynthetically derived organic material in the post-larval and juvenile stages.
More than 2,000 historic shipwrecks spanning 500 years of history, rest on the Gulf of Mexico seafloor. Shipwrecks serve as artificial reefs and hotspots of biodiversity by providing hard substrate, something rare in deep ocean regions. The Deepwater Horizon (DWH) spill discharged crude oil into the deep Gulf. Because of physical, biological, and chemical interactions, DWH oil was deposited on the seafloor, where historic shipwrecks are present. This study examined sediment microbiomes at seven historic shipwrecks. Steel-hulled, World War II-era shipwrecks and wooden-hulled, 19th century shipwrecks within and outside of the surface oiled area and subsurface plume were examined. Analysis of 16S rRNA sequence libraries, sediment radiocarbon age data, sedimentation rates, and hydrocarbons revealed that the German U-boat U-166 and the wooden-hulled sailing vessel known as the Mardi Gras Wreck, both in the Mississippi Canyon leasing area, were exposed to deposited oil during a rapid sedimentation event. Impacts to shipwreck microbiomes included a significant increase in Piscirickettsiaceae-related sequences in surface sediments, and reduced biodiversity relative to unimpacted sites. This study is the first to address the impact of the spill on shipwreck-associated microbiomes, and to explore how shipwrecks themselves influence microbiome diversity in the deep sea.
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.
The release of hydrocarbons and chemical dispersant in marine environments may disrupt benthic ecosystems, including artificial reefs, formed by historic steel shipwrecks, and their associated organisms. Experiments were performed to determine the impacts of crude oil, dispersed crude oil, and dispersant on the community structure and function of microorganisms in seawater (SW) and biofilms formed on carbon steel, a common ship hull construction material. Steel corrosion was also monitored to illustrate how oil spills may impact preservation of steel shipwrecks. Microcosms were filled with seawater (SW) and incubated at 4 • C. Carbon steel disks (CSDs) were placed in each tank, and tanks were amended with crude oil and/or dispersant or no treatment. SW and CSD biofilms were sampled biweekly for genetic analysis using Illumina sequencing of 16S ribosomal RNA gene amplicons. Predicted and sequenced bacterial metagenomes were analyzed to examine impacts of oil and dispersant on metabolic function. Gammaproteobacteria, Alphaproteobacteria, and Flavobacteriia dominated SW and biofilms. Bacterial community structure differed significantly between treatments for SW and biofilms. OTUs affiliated with known (Pseudomonas) and potential (Marinomonas) hydrocarbon-degraders were roughly twice as abundant in biofilms treated with oil and dispersed oil, and steel corrosion of CSDs in these treatments was higher compared to control and dispersant treatments. OTUs affiliated with the Rhodobacteraceae family (biofilm formers and potential oil degraders) were less abundant in the dispersant treatment compared to other treatments in biofilm and SW samples, but OTUs affiliated with the Pseudoalteromonas genus (biofilm formers and proposed hydrocarbon degraders) were more abundant in dispersant-treated biofilms. Overall, functional gene analyses revealed a decrease in genes (predicted using PICRUSt and observed in sequenced metagenomes) associated with hydrocarbon degradation in dispersant-treated biofilms. This study indicates that exposure to oil and dispersant could disrupt the composition and metabolic function of biofilms colonizing metal hulls, as well as corrosion processes, potentially compromising shipwrecks as ecological and historical resources.
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.
Stony coral tissue loss disease (SCTLD) has been causing significant whole colony mortality on reefs in Florida and the Caribbean. The cause of SCTLD remains unknown, with the limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of 16S ribosomal RNA gene datasets generated by 16 field and laboratory SCTLD studies to find consistent bacteria associated with SCTLD across disease zones (vulnerable, endemic, and epidemic), coral species, coral compartments (mucus, tissue, and skeleton), and colony health states (apparently healthy colony tissue (AH), and unaffected (DU) and lesion (DL) tissue from diseased colonies). We also evaluated bacteria in seawater and sediment, which may be sources of SCTLD transmission. Although AH colonies in endemic and epidemic zones harbor bacteria associated with SCTLD lesions, and aquaria and field samples had distinct microbial compositions, there were still clear differences in the microbial composition among AH, DU, and DL in the combined dataset. Alpha-diversity between AH and DL was not different; however, DU showed increased alpha-diversity compared to AH, indicating that, prior to lesion formation, corals may undergo a disturbance to the microbiome. This disturbance may be driven by Flavobacteriales, which were especially enriched in DU. In DL, Rhodobacterales and Peptostreptococcales–Tissierellales were prominent in structuring microbial interactions. We also predict an enrichment of an alpha-toxin in DL samples which is typically found in Clostridia. We provide a consensus of SCTLD-associated bacteria prior to and during lesion formation and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.
Factors driving the distribution of marine microorganisms are widely debated and poorly understood. Recent studies show that free-living marine microbes exhibit geographical patterns indicative of limited dispersal. In contrast, host-associated microbes face a different set of dispersal challenges, and hosts may function as habitat 'islands' for resident microbial populations. Here, we examine the biogeographical distributions of planktonic and adjacent coral-associated bacterial communities across the Hawaiian Archipelago, Johnston Atoll (∼1400 km southwest of Hawaii) and American Samoa in the Pacific Ocean and investigate the potential underlying processes driving observed patterns. Statistical analyses of bacterial community structure, determined using a small-subunit ribosomal RNA gene-based approach, showed that bacterioplankton and coral-associated bacterial communities were distinct, and correlated with geographical distance between sites. In addition, biogeographical patterns of bacterial associates paralleled those of their host coral Porites lobata, highlighting the specificity of these associations and the impact that host dispersal may have on bacterial biogeography. Planktonic and coral-associated bacterial communities from distant Johnston Atoll were shown to be connected with communities from the center of the Hawaiian Archipelago, a pattern previously observed in fish and invertebrates. No significant correlations were detected with habitat type, temperature or depth. However, non-distance-based geographical groupings were detected, indicating that, in addition to dispersal, unidentified environmental factors also affected the distributions of bacterial communities investigated here.
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