Cultivation mutualism between a deep-sea vent galatheid crab and its chemosynthetic epibionts

Watsuji, Tomo‐o; Tsubaki, Remi; Chen, Chong; Nagai, Yukiko; Nakagawa, Satoshi; Yamamoto, Masahiro; Nishiura, Daisuke; Toyofuku, Takashi; Takai, Ken

doi:10.1016/j.dsr.2017.04.012

Cited by 9 publications

(6 citation statements)

References 32 publications

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“…Distinct differences between free-living and decapod-associated microbial communities have been highlighted previously 3 . An alternative source of epibionts often suggested for deep-sea hydrothermal vent crustaceans like R. exoculata , K. hirsuta or S. crosnieri is the horizontal acquisition from conspecifics 9 , 10 , 35 , 36 . This coincides with our findings that microbial communities found on all M. alvisca specimens were highly similar (Fig.…”

Section: Discussionmentioning

confidence: 99%

Microbial epibiotic community of the deep-sea galatheid squat lobster Munidopsis alvisca

Leinberger

Milke

Christodoulou

et al. 2022

Sci Rep

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Life at hydrothermal vent sites is based on chemosynthetic primary producers that supply heterotrophic microorganisms with substrates and generate biomass for higher trophic levels. Often, chemoautotrophs associate with the hydrothermal vent megafauna. To investigate attached bacterial and archaeal communities on deep-sea squat lobsters, we collected ten specimens from a hydrothermal vent in the Guaymas Basin (Gulf of California). All animals were identified as Munidopsis alvisca via morphological and molecular classification, and intraspecific divergence was determined. Amplicon sequencing of microbial DNA and cDNA revealed significant differences between microbial communities on the carapaces of M. alvisca and those in ambient sea water. Major epibiotic bacterial taxa were chemoautotrophic Gammaproteobacteria, such as Thiotrichaceae and Methylococcaceae, while archaea were almost exclusively represented by sequences affiliated with Ca. Nitrosopumilus. In sea water samples, Marine Group II and III archaea and organoheterotrophic Alphaproteobacteria, Flavobacteriia and Planctomycetacia were more dominant. Based on the identified taxa, we assume that main metabolic processes, carried out by M. alvisca epibiota, include ammonia, methane and sulphide oxidation. Considering that M. alvisca could benefit from sulphide detoxification by its epibiota, and that attached microbes are supplied with a stable habitat in proximity to substrate-rich hydrothermal fluids, a mutualistic host-microbe relationship appears likely.

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Section: Discussionmentioning

confidence: 99%

Microbial epibiotic community of the deep-sea galatheid squat lobster Munidopsis alvisca

Leinberger

Milke

Christodoulou

et al. 2022

Sci Rep

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“… Shinkaia crosnieri is a deep-sea invertebrate that predominantly (up to 465 individuals/m 2 ) inhabits an area around hydrothermal vents in the Okinawa Trough in Japan ( 12 ). S. crosnieri utilizes episymbiotic microbes on the surface of its ventral setae as its primary nutrient source, and its symbiotic system is the most clearly characterized one among deep-sea episymbioses ( 13 , 14 ). Those episymbionts were revealed to contain methane-utilizing and sulfur (thiosulfate and sulfide)-oxidizing chemolithotrophic bacteria ( 15 , 16 ).…”

Section: Introductionmentioning

confidence: 99%

Metatranscriptomics by In Situ RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters

et al. 2020

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Shinkaia crosnieri is an invertebrate that inhabits an area around deep-sea hydrothermal vents in the Okinawa Trough in Japan by harboring episymbiotic microbes as the primary nutrition. To reveal physiology and phylogenetic composition of the active episymbiotic populations, metatranscriptomics is expected to be a powerful approach. However, this has been hindered by substantial perturbation (e.g., RNA degradation) during time-consuming retrieval from the deep sea. Here, we conducted direct metatranscriptomic analysis of S. crosnieri episymbionts by applying in situ RNA stabilization equipment. As expected, we obtained RNA expression profiles that were substantially different from those obtained by conventional metatranscriptomics (i.e., stabilization after retrieval). The episymbiotic community members were dominated by three orders, namely, Thiotrichales, Methylococcales, and Campylobacterales, and the Campylobacterales members were mostly dominated by the Sulfurovum genus. At a finer phylogenetic scale, the episymbiotic communities on different host individuals shared many species, indicating that the episymbionts on each host individual are not descendants of a few founder cells but are horizontally exchanged. Furthermore, our analysis revealed the key metabolisms of the community: two carbon fixation pathways, a formaldehyde assimilation pathway, and utilization of five electron donors (sulfide, thiosulfate, sulfur, methane, and ammonia) and two electron accepters (oxygen and nitrate/nitrite). Importantly, it was suggested that Thiotrichales episymbionts can utilize intercellular sulfur globules even when sulfur compounds are not usable, possibly also in a detached and free-living state. IMPORTANCE Deep-sea hydrothermal vent ecosystems remain mysterious. To depict in detail the enigmatic life of chemosynthetic microbes, which are key primary producers in these ecosystems, metatranscriptomic analysis is expected to be a promising approach. However, this has been hindered by substantial perturbation (e.g., RNA degradation) during time-consuming retrieval from the deep sea. In this study, we conducted direct metatranscriptome analysis of microbial episymbionts of deep-sea squat lobsters (Shinkaia crosnieri) by applying in situ RNA stabilization equipment. Compared to conventional metatranscriptomics (i.e., RNA stabilization after retrieval), our method provided substantially different RNA expression profiles. Moreover, we discovered that S. crosnieri and its episymbiotic microbes constitute complex and resilient ecosystems, where closely related but various episymbionts are stably maintained by horizontal exchange and partly by their sulfur storage ability for survival even when sulfur compounds are not usable, likely also in a detached and free-living state.

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“…Kiwa puravida displays a "dancing" behavior suggested to increase the productivity of its bacterial epibionts (Thurber et al, 2011). The importance of water flow for increasing chemosynthetic production from the bacterial epibionts was affirmed in the vent galatheid crab Shinkaia crosnieri (Watsuji et al, 2017). Differences in bacterial composition among body parts and ontogenetic changes in bacterial communities have been observed in K. puravida (Goffredi et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Sexual dimorphism in the methane seep-dwelling Costa Rican yeti crab Kiwa puravida (Decapoda: Anomura: Kiwaidae)

et al. 2022

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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.

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Cultivation mutualism between a deep-sea vent galatheid crab and its chemosynthetic epibionts

Cited by 9 publications

References 32 publications

Microbial epibiotic community of the deep-sea galatheid squat lobster Munidopsis alvisca

Microbial epibiotic community of the deep-sea galatheid squat lobster Munidopsis alvisca

Metatranscriptomics by In Situ RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters

Sexual dimorphism in the methane seep-dwelling Costa Rican yeti crab Kiwa puravida (Decapoda: Anomura: Kiwaidae)

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