scholarly journals A Toll-like receptor identified in Gigantidas platifrons and its potential role in the immune recognition of endosymbiotic methane oxidation bacteria

PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e11282
Author(s):  
Mengna Li ◽  
Hao Chen ◽  
Minxiao Wang ◽  
Zhaoshan Zhong ◽  
Hao Wang ◽  
...  

Symbiosis with chemosynthetic bacteria is an important ecological strategy for the deep-sea megafaunas including mollusks, tubeworms and crustacean to obtain nutrients in hydrothermal vents and cold seeps. How the megafaunas recognize symbionts and establish the symbiosis has attracted much attention. Bathymodiolinae mussels are endemic species in both hydrothermal vents and cold seeps while the immune recognition mechanism underlying the symbiosis is not well understood due to the nonculturable symbionts. In previous study, a lipopolysaccharide (LPS) pull-down assay was conducted in Gigantidas platifrons to screen the pattern recognition receptors potentially involved in the recognition of symbiotic methane-oxidizing bacteria (MOB). Consequently, a total of 208 proteins including GpTLR13 were identified. Here the molecular structure, expression pattern and immune function of GpTLR13 were further analyzed. It was found that GpTLR13 could bind intensively with the lipid A structure of LPS through surface plasmon resonance analysis. The expression alternations of GpTLR13 transcripts during a 28-day of symbiont-depletion assay were investigated by real-time qPCR. As a result, a robust decrease of GpTLR13 transcripts was observed accompanying with the loss of symbionts, implying its participation in symbiosis. In addition, GpTLR13 transcripts were found expressed exclusively in the bacteriocytes of gills of G. platifrons by in situ hybridization. It was therefore speculated that GpTLR13 may be involved in the immune recognition of symbiotic methane-oxidizing bacteria by specifically recognizing the lipid A structure of LPS. However, the interaction between GpTLR13 and symbiotic MOB was failed to be addressed due to the nonculturable symbionts. Nevertheless, the present result has provided with a promising candidate as well as a new approach for the identification of symbiont-related genes in Bathymodiolinae mussels.


2020 ◽  
Author(s):  
Hao Chen ◽  
Minxiao Wang ◽  
Huan Zhang ◽  
Hao Wang ◽  
Li Zhou ◽  
...  

Abstract Background:As the dominant species inhabiting both cold seeps and hydrothermal vents,Bathymodiolinae mussels are one of the most successful megafauna in the deep sea.They thrive in dark and food-insufficient environmentsby harboring sulfur-oxidizing bacteria (SOB)and/or methane-oxidizing bacteria (MOB)ingill bacteriocytesand obtain the majority of their nutrition from them.Many attempts have been made to decode the mechanisms underlying their symbiosis, which yetremained largely undisclosedfor years due to the lack of cultivable symbionts. In the present study,the globalexpression pattern of immune-related genes and miRNAswere surveyed inGigantidasplatifronsduring bacterial challengesusing enriched symbiontsor nonsymbioticVibrio in attempting to reveal the molecular mechanisms underlying chemosynthetic symbiosis. Results: Multiple PRRs such as TLRs, LRRs and C1q were found vigorously modulated during challenges whiledistinctly clusteredbetween symbiotic and nonsymbiotic bacteria stimulation. As downstream of the immune response,dozens of immune effectors including HSP70, P450, CD82 andvacuolar protein sorting-associated proteinwere modulated simultaneously, contributing to the fine tuning of cellular homeostasis, lysosome activity and bacteria engulfment in either symbiotic and nonsymbiotic bacteria challenge.A total of 459 miRNAs were identified in gill tissue of G. platifrons while dozens of themwere differentially expressedduring the challenge.Among these miRNAs, some were also found in differentexpression patternbetween symbiont or nonsymbiontchallenges and targeting apoptosis and phagosome maturation-related genes, including caspase8, inhibitor of apoptosis, cAMP-responsive element-binding protein,IκB, Rab and integrin. Conclusion:It was suggested that G. platifrons PRRs might function cooperativelyto facilitate the specialized immune recognition to MOBs or nonsymbioticbacteria. Meanwhile, a shared expression pattern of immune effectorswas observed between bacterial challenges, indicatingthe conservative response of Bathymodiolinae mussels in promoting the adhesion andengulfment of symbionts and nonsymbiont. Nevertheless, the differentially expressed miRNAs were yet suggested to facilitate specialized modulationinsymbiosis by repressing apoptosis- and phagosome maturation-related genes.With the orchestra of immune-related genes and miRNAs, G. platifronsmussels could therefore maintain arobust immune response against invading pathogens while establishing symbiosis with chemosynthetic bacteria.



Author(s):  
A. J. Southward ◽  
P. R. Dando

The Pogonophora are tube-worms of predominantly deep sea distribution. They lack a functioning alimentary canal in the adult stage and are then dependent for nutrition on internal symbiotic chemosynthetic bacteria that occupy tissue derived from the larval endoderm (Southward, 1982, 1987, 1988; Southward & Southward, 1987; Southwardet al.1981). Of the two main subgroups, the small perviate Pogonophora are widely distributed in reducing sediments in the oceans, while the large vestimentiferan or obturate Pogonophora are restricted to hydrothermal vents or cold seeps. The small Pogonophora are often most abundant on steep slopes and in the Bay of BiscaySiboglinum atlanticum(Southward & Southward, 1958) can be a dominant element of the infauna of the sediments on the sides of canyons. This animal, like other small Pogonophora, lies buried in the sediment, in contrast to the vestimentifera which are attached to hard substrates. Until now there has been no fully quantitative information on the distribution ofS. atlanticumand associated pogonophores of the Bay of Biscay. Dredges or trawls have been used for most previous sampling of pogonophores along the continental slope (Southward, 1979, 1985). Even the Plymouth-pattern deep-sea anchor dredge (Southward & Southward, 1963), which is designed to dig into the sediment immediately it is towed on the bottom, may drag for some distance through soft sediments before digging in, and then samples the upper few centimetres over a wider area than its mouth opening. During the last season of operation of R.R.S. ‘Frederick Russell’, before this vessel was disposed of by N.E.R.C., opportunity was taken to make a combined quantitative biological and chemical survey, using box-corers. The samples from the corers were large enough to allow the sample to be used for assessment of the population density of the pogonophores and analysis of sediment chemistry. Some inferences can now be drawn about the factors controlling pogonophore abundance.



Author(s):  
Jack Chi-Ho Ip ◽  
Ting Xu ◽  
Jin Sun ◽  
Runsheng Li ◽  
Chong Chen ◽  
...  

Abstract Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.



2020 ◽  
Vol 32 (5) ◽  
pp. 354-366
Author(s):  
Chong Chen ◽  
Katrin Linse

AbstractLush ‘oases’ of life seen in chemosynthetic ecosystems such as hot vents and cold seeps represent rare, localized exceptions to the generally oligotrophic deep ocean floor. Organic falls, best known from sunken wood and whale carcasses, are additional sources of such oases. Kemp Caldera (59°42'S, 28°20'W) in the Weddell Sea exhibits active hydrothermal vents and a natural whale fall in close proximity, where an undescribed cocculinid limpet was found living in both types of chemosynthetic habitats. This represents the first member of the gastropod order Cocculinida discovered from hot vents, and also the first record from the Southern Ocean. Here, we applied an integrative taxonomy framework incorporating traditional dissection, electron microscopy, genetic sequencing and 3D anatomical reconstruction through synchrotron computed tomography in order to characterize this species. Together, our data revealed an unusual member of the genus Cocculina with a highly modified radula for feeding on bacterial film, described herein as Cocculina enigmadonta n. sp. Its phylogenetically derived position within the largely wood-inhabiting Cocculina indicates that it probably evolved from an ancestor adapted to living on sunken wood, providing a compelling case of the ‘stepping stone’ evolutionary trajectory from organic falls to seeps and vents.





2017 ◽  
Vol 4 ◽  
Author(s):  
Perrine Cruaud ◽  
Adrien Vigneron ◽  
Patricia Pignet ◽  
Jean-Claude Caprais ◽  
Françoise Lesongeur ◽  
...  


Author(s):  
Sabine Stöhr ◽  
Michel Segonzac

The animal communities associated with the deep-sea reducing environment have been studied for almost 30 years, but until now only a single species of ophiuroid, Ophioctenella acies, has been found at both hydrothermal vents and methane cold seeps. Since the faunal overlap between vent and seep communities is small and many endemic species have been found among other taxa (e.g. Mollusca, Crustacea), additional species of ophiuroids were expected at previously unstudied sites. Chemical compositions at reducing sites differ greatly from the nearby bathyal environment. Generally, species adapted to chemosynthetic environments are not found in non-chemosynthetic habitats, but occasional visitors of other bathyal species to vent and seep sites have been recorded among many taxa except ophiuroids. This paper presents an analysis of the ophiuroid fauna found at hydrothermal vents and non-reducing nearby sites on the Mid-Atlantic Ridge and on methane cold seeps in the Gulf of Mexico, at Blake Ridge off South Carolina and south of Barbados. In addition to O. acies, four species were found at vents, Ophiactis tyleri sp. nov., Ophiocten centobi, Ophiomitra spinea and Ophiotreta valenciennesi rufescens. While Ophioctenella acies appears to be restricted to chemosynthetic areas, the other four species were also found in other bathyal habitats. They also occur in low numbers (mostly single individuals), whereas species adapted to hydrothermal areas typically occur in large numbers. Ophioscolex tripapillatus sp. nov. and Ophiophyllum atlanticum sp. nov. are described from nearby non-chemosynthetic sites. In a cold seep south of Barbados, three species of ophiuroids were found, including Ophioctenella acies, Amphiura sp., Ophiacantha longispina sp. nov. and Ophioplinthaca chelys. From the cold seeps at Blake Ridge and the Gulf of Mexico, Ophienigma spinilimbatum gen. et sp. nov. is described, likely restricted to the reducing environment. Ophiotreta valenciennesi rufescens occurred abundantly among Lophelia corals in the Gulf of Mexico seeps, which is the first record of this species from the West Atlantic. Habitat descriptions complement the taxonomic considerations, and the distribution of the animals in reducing environments is discussed.



JOM ◽  
2015 ◽  
Vol 67 (11) ◽  
pp. 2494-2501
Author(s):  
Jenifer K. Tucker ◽  
Mark L. Richter ◽  
Cindy L. Berrie


1998 ◽  
Vol 1373 (1) ◽  
pp. 101-111 ◽  
Author(s):  
Matthew A. Cooper ◽  
Andrew C. Try ◽  
Joe Carroll ◽  
David J. Ellar ◽  
Dudley H. Williams


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