Methane-powered sea spiders: Diverse, epibiotic methanotrophs serve as a source of nutrition for deep-sea methane seep Sericosura

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.

We thank the captains and crew of the R/V Atlantis, HOV Alvin pilots and technicians, as well as scientific participants of expeditions AT50-12 and AT50-24, especially Dr. Tina Truede, a principal investigator on both expeditions, Rebecca Wipfler, Dan Utter, Ruby Siehl, Charlotte Seid, and Greg Rouse for support at sea, as well as the captains and crew of the R/V Western Flyer with ROV Doc Ricketts and scientific participants of expedition WF05-21. We also thank Ralph Appy and G. Rouse for SEM assistance, Angelica Bradley and Rachel Survilas for stable isotope sample processing in the laboratory, and Stephanie Connon for assistance with microbial community analysis. Dr. Maxim Rubin Blum (Israel Oceanographic and Limnological Research), Haifa Israel provided additional Hymedesmia sponge 16S rRNA sequences. Dr. Kai-Uwe Hinrichs (University of Bremen, MARUM & Department of Geosciences) provided advice on ¹³C enrichment mixed modeling. We thank Emmanuelle Botté from Manuscribe for support in editing this manuscript. Support for undergraduate participation was provided by Ron and Susan Hahn and the Science Scholars Program at Occidental College, funded by the Fletcher Jones Foundation and administered through the Undergraduate Research Center. Funding for this project was made possible by the US NSF grants OCE-2048481 (S.K.G.), OCE-2048720 (L.A.L.) and OCE-2048666 (V.J.O.).