Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters

ABSTRACT 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, metatranscript...

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Autores principales:	Kaori Motoki, Tomo-o Watsuji, Yoshihiro Takaki, Ken Takai, Wataru Iwasaki
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	chemosynthesis deep sea in situ analysis metatranscriptome symbiosis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e242d7fbd47340aa9d5256b5227ab473
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spelling	oai:doaj.org-article:e242d7fbd47340aa9d5256b5227ab4732021-12-02T19:47:36ZMetatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters10.1128/mSystems.00551-202379-5077https://doaj.org/article/e242d7fbd47340aa9d5256b5227ab4732020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00551-20https://doaj.org/toc/2379-5077ABSTRACT 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.Kaori MotokiTomo-o WatsujiYoshihiro TakakiKen TakaiWataru IwasakiAmerican Society for Microbiologyarticlechemosynthesisdeep seain situ analysismetatranscriptomesymbiosisMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	chemosynthesis deep sea in situ analysis metatranscriptome symbiosis Microbiology QR1-502
spellingShingle	chemosynthesis deep sea in situ analysis metatranscriptome symbiosis Microbiology QR1-502 Kaori Motoki Tomo-o Watsuji Yoshihiro Takaki Ken Takai Wataru Iwasaki Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters
description	ABSTRACT 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.
format	article
author	Kaori Motoki Tomo-o Watsuji Yoshihiro Takaki Ken Takai Wataru Iwasaki
author_facet	Kaori Motoki Tomo-o Watsuji Yoshihiro Takaki Ken Takai Wataru Iwasaki
author_sort	Kaori Motoki
title	Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters
title_short	Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters
title_full	Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters
title_fullStr	Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters
title_full_unstemmed	Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters
title_sort	metatranscriptomics by <italic toggle="yes">in situ</italic> rna stabilization directly and comprehensively revealed episymbiotic microbial communities of deep-sea squat lobsters
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/e242d7fbd47340aa9d5256b5227ab473
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Metatranscriptomics by <italic toggle="yes">In Situ</italic> RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters

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