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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. 

The methane seeps on the Pacific margin of Costa Rica support extensive animal diversity and offer insights into deep-sea biogeography. During five expeditions between 2009 and 2019, we conducted intensive faunal sampling via 63 submersible dives to 11 localities at depths of 300–3600 m. Based on these expeditions and published literature, we compiled voucher specimens, images, and 274 newly published DNA sequences to present a taxonomic inventory of macrofaunal and megafaunal diversity with a focus on invertebrates. In total 488 morphospecies were identified, representing the highest number of distinct morphospecies published from a single seep or vent region to date. Of these, 131 are described species, at least 58 are undescribed species, and the remainder include some degree of taxonomic uncertainty, likely representing additional undescribed species. Of the described species, 38 are known only from the Costa Rica seeps and their vicinity. Fifteen range extensions are also reported for species known from Mexico, the Galápagos seamounts, Chile, and the western Pacific; as well as 16 new depth records and three new seep records for species known to occur at vents or organic falls. No single evolutionary narrative explains the patterns of biodiversity at these seeps, as even morphologically indistinguishable species can show different biogeographic affinities, biogeographic ranges, or depth ranges. The value of careful molecular taxonomy and comprehensive specimen-based regional inventories is emphasized for biodiversity research and monitoring. 

Pterobdella occidentalis n. sp. (Hirudinida: Piscicolidae) is described from the longjaw mudsucker, Gillichthys mirabilis Cooper, 1864, and the staghorn sculpin, Leptocottus armatus Girard, 1854, in the eastern Pacific, and the diagnosis of Pterobdella abditovesiculata (Moore, 1952) from the ‘o‘opu ‘akupa, Eleotris sandwicensis Vaillant and Sauvage, 1875, from Hawaii is amended. The morphology of both species conforms with the genus Pterobdella in possessing a spacious coelom, well-developed nephridial system, and 2 pairs of mycetomes. Originally described as Aestabdella abditovesiculata, P. occidentalis (present along the U.S. Pacific Coast), can be distinguished from most congeners by its metameric pigmentation pattern and diffuse pigmentation on the caudal sucker. Based on mitochondrial gene sequences, including cytochrome c oxidase subunit I (COI) and NADH dehydrogenase subunit I (ND1), P. occidentalis forms a distinct polyphyletic clade with Pterobdella leiostomi from the western Atlantic. Based on COI, ND1, and the 18S rRNA genes, other leech species most closely related to P. occidentalis include Pterobdella arugamensis from Iran, Malaysia, and possibly Borneo, which likely represent distinct species, and Pterobdella abditovesiculata from Hawaii, one of only a few endemic fish parasites in Hawaii. Like P. abditovesiculata, P. arugamensis, and Petrobdella amara, P. occidentalis is often found in estuarine environments, frequently infecting hosts adapted to a wide range of salinity, temperature, and oxygen. The physiological plasticity of P. occidentalis and the longjaw mudsucker host, and the ease of raising P. occidentalis in the lab, make it an excellent candidate for the study of leech physiology, behavior, and possible bacterial symbionts. 

Persistent bacterial presence is believed to play an important role in host adaptation to specific niches that would otherwise be unavailable, including the exclusive consumption of blood by invertebrate parasites. Nearly all blood-feeding animals examined so far host internal bacterial symbionts that aid in some essential aspect of their nutrition. Obligate blood-feeding (OBF) invertebrates exist in the oceans, yet symbiotic associations between them and beneficial bacteria have not yet been explored. This study describes the microbiome of 6 phylogenetically-diverse species of marine obligate blood-feeders, including leeches (both fish and elasmobranch specialists; e.g., Pterobdella, Ostreobdella, and Branchellion ), isopods (e.g., Elthusa and Nerocila ), and a copepod (e.g., Lernanthropus ). Amplicon sequencing analysis revealed the blood-feeding invertebrate microbiomes to be low in diversity, compared to host fish skin surfaces, seawater, and non-blood-feeding relatives, and dominated by only a few bacterial genera, including Vibrio (100% prevalence and comprising 39%–81% of the average total recovered 16S rRNA gene sequences per OBF taxa). Vibrio cells were localized to the digestive lumen in and among the blood meal for all taxa examined via fluorescence microscopy. For Elthusa and Branchellion, Vibrio cells also appeared intracellularly within possible hemocytes, suggesting an interaction with the immune system. Additionally, Vibrio cultivated from four of the obligate blood-feeding marine taxa matched the dominant amplicons recovered, and all but one was able to effectively lyse vertebrate blood cells. Bacteria from 2 additional phyla and 3 families were also regularly recovered, albeit in much lower abundances, including members of the Oceanospirillaceae, Flavobacteriacea, Porticoccaceae, and unidentified members of the gamma-and betaproteobacteria, depending on the invertebrate host. For the leech Pterobdella , the Oceanospirillaceae were also detected in the esophageal diverticula. For two crustacean taxa, Elthusa and Lernanthropus , the microbial communities associated with brooded eggs were very similar to the adults, indicating possible direct transmission. Virtually nothing is known about the influence of internal bacteria on the success of marine blood-feeders, but this evidence suggests their regular presence in marine parasites from several prominent groups. 

Deep-sea chemosynthesis-based ecosystems support unique biological communities, but human impacts are an increasing threat. Understanding the life-history traits of species from deep-sea chemosynthesis-based ecosystems can help to develop adequate management strategies, as these can have impacts on ecological responses to changes in the environment. Here we examined the occurrence of sexual dimorphism in the yeti crab Kiwa puravida , an endemic species from the Costa Rican Pacific margin that aggregates at active methane seeps and depends on chemosynthetic bacteria for nutrition. The two morphological features examined included the claws, suspected to be under sexual selection and used for defense, and the carpus of the second pereopod not suspected to be under sexual selection. A total of 258 specimens, 161 males, 81 females, 16 juveniles, were collected from Mound 12 at 1,000-1,040 m depth in 2017 and 2018 and analyzed. We found that males have larger and wider claws than females, while there were no differences in carpus length. These results suggest that claw weaponry is under sexual selection in K . puravida , which is probably related to the mating system of this deep-sea species. This is the first attempt to study the reproductive biology of K . puravida , and additional observations will be necessary to shed more light on this matter. 

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.