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Methane seeps harbor uncharacterized animal–microbe symbioses with unique nutritional strategies. Three undescribed sea spider species (family Ammotheidae; genusSericosura) endemic to methane seeps were found along the eastern Pacific margin, from California to Alaska, hosting diverse methane- and methanol-oxidizing bacteria on their exoskeleton. δ13C tissue isotope values of in situ specimens corroborated methane assimilation (−45‰, on average). Live animal incubations with13C-labeled methane and methanol, followed by nanoscale secondary ion mass spectrometry, confirmed that carbon derived from both compounds was actively incorporated into the tissues within five days. Methano- and methylotrophs of the bacterial families Methylomonadaceae, Methylophagaceae and Methylophilaceae were abundant, based on environmental metagenomics and 16S rRNA sequencing, and fluorescence and electron microscopy confirmed dense epibiont aggregations on the sea spider exoskeleton. Egg sacs carried by the males hosted identical microbes suggesting vertical transmission. We propose that these sea spiders farm and feed on methanotrophic and methylotrophic bacteria, expanding the realm of animals known to harness C1 compounds as a carbon source. These findings advance our understanding of the biology of an understudied animal lineage, unlocking some of the unique nutritional links between the microbial and faunal food webs in the oceans.
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Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage
Deep-sea cold seeps are dynamic sources of methane release and unique habitats supporting ocean biodiversity and productivity. Here, we describe newly discovered animal-bacterial symbioses fueled by methane, between two species of annelid (a serpulid Laminatubus and sabellid Bispira ) and distinct aerobic methane-oxidizing bacteria belonging to the Methylococcales, localized to the host respiratory crown. Worm tissue δ 13 C of −44 to −58‰ are consistent with methane-fueled nutrition for both species, and shipboard stable isotope labeling experiments revealed active assimilation of 13 C-labeled methane into animal biomass, which occurs via the engulfment of methanotrophic bacteria across the crown epidermal surface. These worms represent a new addition to the few animals known to intimately associate with methane-oxidizing bacteria and may further explain their enigmatic mass occurrence at 150–million year–old fossil seeps. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep sea and, by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.
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- PAR ID:
- 10192016
- Date Published:
- Journal Name:
- Science Advances
- Volume:
- 6
- Issue:
- 14
- ISSN:
- 2375-2548
- Page Range / eLocation ID:
- eaay8562
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Methane seeps harbor uncharacterized animal–microbe symbioses with unique nutritional strategies. Three undescribed sea spider species (family Ammotheidae; genus Sericosura) endemic to methane seeps were found along the eastern Pacific margin, from California to Alaska, hosting diverse methane-and methanol-oxidizing bacteria on their exoskeleton. δ13C tissue isotope values of in situ specimens corroborated methane assimilation (−45‰, on average). Live animal incubations with 13C-labeled methane and methanol, followed by nanoscale secondary ion mass spectrometry, confirmed that carbon derived from both compounds was actively incorporated into the tissues within five days. Methano-and methylotrophs of the bacterial families Methylomonadaceae, Methylophagaceae and Methylophilaceae were abundant, based on environmental metagenomics and 16S rRNA sequencing, and fluorescence and electron microscopy confirmed dense epibiont aggregations on the sea spider exoskeleton. Egg sacs carried by the males hosted identical microbes suggesting vertical transmission. We propose that these sea spiders farm and feed on methanotrophic and methylotrophic bacteria, expanding the realm of animals known to harness C1 compounds as a carbon source. These findings advance our understanding of the biology of an understudied animal lineage, unlocking some of the unique nutritional links between the microbial and faunal food webs in the oceans.more » « less
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Methane seeps provide biogeochemical and microbial heterogeneity in deep-sea habitats. In the Northeast (NE) Pacific Ocean recent studies have found an abundance of seeps at varying spatial separations and within distinct biogeochemical environments ranging in oxygen, depth, and temperature. Here, we examine eight newly discovered seeps and two known seeps covering 800 km and varying across 2000 m water depth to identify: (1) novel megafaunal communities in this geographical region; (2) variations in the microbiome of seep habitats across the margin; (3) spatial and biogeochemical drivers of microbial diversity at seeps. In addition to authigenic carbonates, clam beds, microbial mats, and exposed hydrates - we also observed Siboglinidae tube worm bushes and an anomalous deep-sea barnacle adding to the overall habitats known from the NE Pacific. The microbial communities showed high variability in their spatial distribution and community structure. The seep communities formed distinct groups that included multiple groups of anaerobic methane oxidizing Archaea (ANME; 1, 2ab, 2c, and 3), often co-occurring within one site – however, there were also other sites with clearly dominant members (e.g. ANME-1s at Nehalem Bank). Sulfide oxidizers were dominated by the non-mat forming Campylobacterales and even though vertical gradients in redox potential typify seep sediments, in two cases there was not a significant change in community structure across the top five cm of sediment. We posit that these patterns were driven by ‘bubble-turbation,’ and bioirrigation by megafauna. A surprising latitudinal trend was observed in species diversity and richness with increasing richness significantly correlated to increasing latitude. Overall, our results demonstrate that heterogeneity is ubiquitous in the seep biome, spanning all faunal classes, and that the understanding of seeps and the drivers of the community structure can be improved by studying seeps at a range of spatial scales.more » « less
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Methane seeps are highly abundant marine habitats that contribute sources of chemosynthetic primary production to marine ecosystems. Seeps also factor into the global budget of methane, a potent greenhouse gas. Because of these factors, methane seeps influence not only local ocean ecology, but also biogeochemical cycles on a greater scale. Methane seeps host specialized microbial communities that vary significantly based on geography, seep gross morphology, biogeochemistry, and a diversity of other ecological factors including cross-domain species interactions. In this study, we collected sediment cores from six seep and non-seep locations from Grays and Quinault Canyons (46–47°N) off Washington State, USA, as well as one non-seep site off the coast of Oregon, USA (45°N) to quantify the scale of seep influence on biodiversity within marine habitats. These samples were profiled using 16S rRNA gene sequencing. Predicted gene functions were generated using the program PICRUSt2, and the community composition and predicted functions were compared among samples. The microbial communities at seeps varied by seep morphology and habitat, whereas the microbial communities at non-seep sites varied by water depth. Microbial community composition and predicted gene function clearly transitioned from on-seep to off-seep in samples collected from transects moving away from seeps, with a clear ecotone and high diversity where methane-fueled habitats transition into the non-seep deep sea. Our work demonstrates the microbial and metabolic sphere of influence that extends outwards from methane seep habitats.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1126/sciadv.aay8562
