“Candidatus Desulfobulbus rimicarensis,” an Uncultivated Deltaproteobacterial Epibiont from the Deep-Sea Hydrothermal Vent Shrimp Rimicaris exoculata

ABSTRACT The deep-sea hydrothermal vent shrimp Rimicaris exoculata largely depends on a dense epibiotic chemoautotrophic bacterial community within its enlarged cephalothoracic chamber. However, our understanding of shrimp-bacterium interactions is limited. In this report, we focused on the deltaproteobacterial epibiont of R. exoculata from the relatively unexplored South Mid-Atlantic Ridge. A nearly complete genome of a Deltaproteobacteria epibiont was binned from the assembled metagenome. Whole-genome phylogenetic analysis reveals that it is affiliated with the genus Desulfobulbus, representing a potential novel species for which the name “Candidatus Desulfobulbus rimicarensis” is proposed. Genomic and transcriptomic analyses reveal that this bacterium utilizes the Wood-Ljungdahl pathway for carbon assimilation and harvests energy via sulfur disproportionation, which is significantly different from other shrimp epibionts. Additionally, this epibiont has putative nitrogen fixation activity, but it is extremely active in directly taking up ammonia and urea from the host or vent environments. Moreover, the epibiont could be distinguished from its free-living relatives by various features, such as the lack of chemotaxis and motility traits, a dramatic reduction in biosynthesis genes for capsular and extracellular polysaccharides, enrichment of genes required for carbon fixation and sulfur metabolism, and resistance to environmental toxins. Our study highlights the unique role and symbiotic adaptation of Deltaproteobacteria in deep-sea hydrothermal vent shrimps. IMPORTANCE The shrimp Rimicaris exoculata represents the dominant faunal biomass at many deep-sea hydrothermal vent ecosystems along the Mid-Atlantic Ridge. This organism harbors dense bacterial epibiont communities in its enlarged cephalothoracic chamber that play an important nutritional role. Deltaproteobacteria are ubiquitous in epibiotic communities of R. exoculata, and their functional roles as epibionts are based solely on the presence of functional genes. Here, we describe “Candidatus Desulfobulbus rimicarensis,” an uncultivated deltaproteobacterial epibiont. Compared to campylobacterial and gammaproteobacterial epibionts of R. exoculata, this bacterium possessed unique metabolic pathways, such as the Wood-Ljungdahl pathway, as well as sulfur disproportionation and nitrogen fixation pathways. Furthermore, this epibiont can be distinguished from closely related free-living Desulfobulbus strains by its reduced genetic content and potential loss of functions, suggesting unique adaptations to the shrimp host. This study is a genomic and transcriptomic analysis of a deltaproteobacterial epibiont and largely expands the understanding of its metabolism and adaptation to the R. exoculata host.

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Identification and Characterization of Carboxyl Esterases of Gill Chamber-Associated Microbiota in the Deep-Sea Shrimp Rimicaris exoculata by Using Functional Metagenomics

Applied and Environmental Microbiology ◽

10.1128/aem.03387-14 ◽

2015 ◽

Vol 81 (6) ◽

pp. 2125-2136 ◽

Cited By ~ 22

Author(s):

María Alcaide ◽

Anatoli Tchigvintsev ◽

Mónica Martínez-Martínez ◽

Ana Popovic ◽

Oleg N. Reva ◽

...

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Metagenomic Library ◽

Content Type ◽

Rimicaris Exoculata ◽

Highly Active ◽

Gill Chamber ◽

Unknown Species ◽

Mid Atlantic Ridge

ABSTRACTThe shrimpRimicaris exoculatadominates the fauna in deep-sea hydrothermal vent sites along the Mid-Atlantic Ridge (depth, 2,320 m). Here, we identified and biochemically characterized three carboxyl esterases from microbial communities inhabiting theR. exoculatagill that were isolated by naive screens of a gill chamber metagenomic library. These proteins exhibit low to moderate identity to known esterase sequences (≤52%) and to each other (11.9 to 63.7%) and appear to have originated from unknown species or from genera ofProteobacteriarelated toThiothrix/Leucothrix(MGS-RG1/RG2) and to theRhodobacteraceaegroup (MGS-RG3). A library of 131 esters and 31 additional esterase/lipase preparations was used to evaluate the activity profiles of these enzymes. All 3 of these enzymes had greater esterase than lipase activity and exhibited specific activities with ester substrates (≤356 U mg−1) in the range of similar enzymes. MGS-RG3 was inhibited by salts and pressure and had a low optimal temperature (30°C), and its substrate profile clustered within a group of low-activity and substrate-restricted marine enzymes. In contrast, MGS-RG1 and MGS-RG2 were most active at 45 to 50°C and were salt activated and barotolerant. They also exhibited wider substrate profiles that were close to those of highly active promiscuous enzymes from a marine hydrothermal vent (MGS-RG2) and from a cold brackish lake (MGS-RG1). The data presented are discussed in the context of promoting the examination of enzyme activities of taxa found in habitats that have been neglected for enzyme prospecting; the enzymes found in these taxa may reflect distinct habitat-specific adaptations and may constitute new sources of rare reaction specificities.

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Novel Bacterial and Archaeal Lineages from an In Situ Growth Chamber Deployed at a Mid-Atlantic Ridge Hydrothermal Vent

Applied and Environmental Microbiology ◽

10.1128/aem.66.9.3798-3806.2000 ◽

2000 ◽

Vol 66 (9) ◽

pp. 3798-3806 ◽

Cited By ~ 273

Author(s):

Anna-Louise Reysenbach ◽

Krista Longnecker ◽

Julie Kirshtein

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrogen Oxidation ◽

Sulfur Metabolism ◽

Rrna Genes ◽

Growth Chamber ◽

In Situ Growth ◽

Small Subunit Rrna ◽

Mid Atlantic Ridge

ABSTRACT The phylogenetic diversity was determined for a microbial community obtained from an in situ growth chamber placed on a deep-sea hydrothermal vent on the Mid-Atlantic Ridge (23Ã¯Â¿Â½22′ N, 44Ã¯Â¿Â½57′ W). The chamber was deployed for 5 days, and the temperature within the chamber gradually decreased from 70 to 20Ã¯Â¿Â½C. Upon retrieval of the chamber, the DNA was extracted and the small-subunit rRNA genes (16S rDNA) were amplified by PCR using primers specific for theArchaea or Bacteria domain and cloned. Unique rDNA sequences were identified by restriction fragment length polymorphisms, and 38 different archaeal and bacterial phylotypes were identified from the 85 clones screened. The majority of the archaeal sequences were affiliated with the Thermococcales (71%) and Archaeoglobales (22%) orders. A sequence belonging to the Thermoplasmales confirms that thermoacidophiles may have escaped enrichment culturing attempts of deep-sea hydrothermal vent samples. Additional sequences that represented deeply rooted lineages in the low-temperature eurarchaeal (marine group II) and crenarchaeal clades were obtained. The majority of the bacterial sequences obtained were restricted to the Aquificales(18%), the ɛ subclass of the Proteobacteria(ɛ-Proteobacteria) (40%), and the genusDesulfurobacterium (25%). Most of the clones (28%) were confined to a monophyletic clade within the ɛ-Proteobacteria with no known close relatives. The prevalence of clones related to thermophilic microbes that use hydrogen as an electron donor and sulfur compounds (S0, SO4, thiosulfate) indicates the importance of hydrogen oxidation and sulfur metabolism at deep-sea hydrothermal vents. The presence of sequences that are related to sequences from hyperthermophiles, moderate thermophiles, and mesophiles suggests that the diversity obtained from this analysis may reflect the microbial succession that occurred in response to the shift in temperature and possible associated changes in the chemistry of the hydrothermal fluid.

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Microbial diversity in deep-sea sediments from the Menez Gwen hydrothermal vent system of the Mid-Atlantic Ridge

Marine Genomics ◽

10.1016/j.margen.2015.09.001 ◽

2015 ◽

Vol 24 ◽

pp. 343-355 ◽

Cited By ~ 24

Author(s):

Teresa Cerqueira ◽

Diogo Pinho ◽

Conceição Egas ◽

Hugo Froufe ◽

Bjørn Altermark ◽

...

Keyword(s):

Microbial Diversity ◽

Deep Sea ◽

Hydrothermal Vent ◽

Deep Sea Sediments ◽

Mid Atlantic Ridge ◽

Menez Gwen

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Ultrastructural characteristics of spermatogenesis in three species of deep-sea hydrothermal vent mytilids

Canadian Journal of Zoology ◽

10.1139/z97-039 ◽

1997 ◽

Vol 75 (2) ◽

pp. 308-316 ◽

Cited By ~ 22

Author(s):

Marcel Le Pennec ◽

Peter G. Beninger

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

The North ◽

Male Gametes ◽

Bathymodiolus Thermophilus ◽

Nutritional Biology ◽

Protandric Hermaphroditism ◽

Mid Atlantic Ridge ◽

Ultrastructural Characteristics ◽

Species Specific

To enhance our understanding of the reproductive biology of deep-sea hydrothermal vent mytilids, the histology of the male gonad and the ultrastructure of its gametes were studied in Bathymodiolus thermophilus, B. puteoserpentis, and B. elongatus. Specimens of B. thermophilus were collected at the 13°N site on the East Pacific ridge, while B. puteoserpentis were sampled from the Snake Pit site of the mid-Atlantic ridge and B. elongatus were obtained from the North Fiji Basin. Gonad histology conformed to the typical bivalve profile; the differences in the proportions of acinal and interacinal tissue, as well as differences in acinal fullness in B. puteoserpentis, indicate that gametogenesis is discontinuous in these deep-sea mytilids. Evidence of protandric hermaphroditism was observed in B. elongatus, which exhibited acini containing both maturing and residual male gametes and immature oocytes. The ultrastructural characteristics of the male gametes conform to those described for littoral bivalve species, and the spermatozoon is of the primitive type. No species-specific differences in spermatozoon ultrastructure were discerned. No evidence of bacterial inclusions was found in either the gametes or the associated gonad cells in any of the species examined. The male gametes are thus probably not vectors for the endosymbiotic bacteria that characterize the nutritional biology of the adults in this genus.

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Characterization of DNA polymerase δ from deep-sea hydrothermal vent shrimp Rimicaris exoculata

Acta Oceanologica Sinica ◽

10.1007/s13131-021-1823-1 ◽

2021 ◽

Vol 40 (8) ◽

pp. 168-175

Author(s):

Wenlin Wu ◽

Hongyun Li ◽

Tiantian Ma ◽

Xiaobo Zhang

Keyword(s):

Dna Polymerase ◽

Deep Sea ◽

Hydrothermal Vent ◽

Dna Polymerase Δ ◽

Rimicaris Exoculata

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Periodic deep‐sea hydrothermal vent activities observed by hydrophones at Mariana, Okinawa, and Mid‐Atlantic Ridge

The Journal of the Acoustical Society of America ◽

10.1121/1.417778 ◽

1996 ◽

Vol 100 (4) ◽

pp. 2639-2639

Author(s):

Kasahara Junzo ◽

Sato Toshinori ◽

Nishizawa Azusa ◽

Fujioka Kantaro

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Mid Atlantic Ridge

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

mSystems ◽

10.1128/msystems.00551-20 ◽

2020 ◽

Vol 5 (5) ◽

Author(s):

Kaori Motoki ◽

Tomo-o Watsuji ◽

Yoshihiro Takaki ◽

Ken Takai ◽

Wataru Iwasaki

Keyword(s):

Deep Sea ◽

Expression Profiles ◽

Rna Degradation ◽

Rna Expression ◽

Free Living ◽

Content Type ◽

Living State ◽

Rna Stabilization ◽

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, 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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