Site-related differences in gene expression and bacterial densities in the mussel Bathymodiolus azoricus from the Menez Gwen and Lucky Strike deep-sea hydrothermal vent sites

Bettencourt, Raúl; Rodrigues, Moacyr Tadeu Vicente; Barros, Inês; Cerqueira, T.; Freitas, Cátia; Costa, Valentina; Pinheiro, Miguel; Egas, Conceição; Santos, Ricardo Serrão

doi:10.1016/j.fsi.2014.05.024

Cited by 18 publications

(11 citation statements)

References 33 publications

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“…The C-type lectin domain (CLECT) characterizes both collectins and the vertebrate mannose-binding lectins able to trigger the lectin pathway of the complement system. CTLs have been associated to agglutination and opsonization of pathogens or parasites in different bivalves [42e44] and the upregulation of their expression has been documented in the hemocytes of clams infected with Perkinsus olseni and in the gills of Bathymodiolus azoricus exposed by immersion to Vibrio parahaemolyticus [45,46].…”

Section: Extracellular Prrsmentioning

confidence: 99%

“…Peptidoglycan recognition receptors (PGRPs) are important PRRs present in all metazoans and able to recognize bacteria by specifically binding PGN, a major component of cell bacterial walls [102]. PGRPs have been characterized in many bivalve species, including scallops, oysters, razor clams [103e105] and the deep-sea hydrothermal vent mussel B. azoricus, where a PGRP was found to be highly abundant in the gills, which typically host edosymbiotic bacteria [46,106]. So far, all these proteins have been regarded as short-type PGRPs for extracellular bacteria recognition.…”

Section: Membrane-bound Prrs and Downstream Signalingmentioning

confidence: 99%

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An updated molecular basis for mussel immunity

Gerdol

Venier

2015

Fish & Shellfish Immunology

134

163

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Non-self recognition with the consequent tolerance or immune reaction is a crucial process to succeed as living organisms. At the same time the interactions between host species and their microbiome, including potential pathogens and parasites, significantly contribute to animal life diversity. Marine filter-feeding bivalves, mussels in particular, can survive also in heavily anthropized coastal waters despite being constantly surrounded by microorganisms. Based on the first outline of the Mytilus galloprovincialis immunome dated 2011, the continuously growing transcript data and the recent release of a draft mussel genome, we explored the available sequence data and scientific literature to reinforce our knowledge on the main gene-encoded elements of the mussel immune responses, from the pathogen recognition to its clearance. We carefully investigated molecules specialized in the sensing and targeting of potential aggressors, expected to show greater molecular diversification, and outlined, whenever relevant, the interconnected cascades of the intracellular signal transduction. Aiming to explore the diversity of extracellular, membrane-bound and intracellular pattern recognition receptors in mussel, we updated a highly complex immune system, comprising molecules which are described here in detail for the first time (e.g. NOD-like receptors) or which had only been partially characterized in bivalves (e.g. RIG-like receptors). Overall, our comparative sequence analysis supported the identification of over 70 novel full-length immunity-related transcripts in M. galloprovincialis. Nevertheless, the multiplicity of gene functions relevant to immunity, the involvement of part of them in other vital processes, and also the lack of a refined mussel genome make this work still not-exhaustive and support the development of more specific studies.

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Section: Extracellular Prrsmentioning

confidence: 99%

Section: Membrane-bound Prrs and Downstream Signalingmentioning

confidence: 99%

An updated molecular basis for mussel immunity

Gerdol

Venier

2015

Fish & Shellfish Immunology

134

163

View full text Add to dashboard Cite

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“…PGRPs were first described as an important component of the innate immune defense [61], but are now known to play a major role in many animal-bacteria symbioses, mediating symbiont tolerance [62, 63], controlling symbiont populations [64], and regulating symbiosis establishment and maintenance [63, 65]. Elevated expression of PGRPs was also observed in the symbiont-bearing tissues of hydrothermal vent tube worms and mussels; however their precise function within these symbioses remains unknown [4, 66]. …”

Section: Resultsmentioning

confidence: 99%

Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis

et al. 2016

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BackgroundThe gutless marine worm Olavius algarvensis has a completely reduced digestive and excretory system, and lives in an obligate nutritional symbiosis with bacterial symbionts. While considerable knowledge has been gained of the symbionts, the host has remained largely unstudied. Here, we generated transcriptomes and proteomes of O. algarvensis to better understand how this annelid worm gains nutrition from its symbionts, how it adapted physiologically to a symbiotic lifestyle, and how its innate immune system recognizes and responds to its symbiotic microbiota.ResultsKey adaptations to the symbiosis include (i) the expression of gut-specific digestive enzymes despite the absence of a gut, most likely for the digestion of symbionts in the host's epidermal cells; (ii) a modified hemoglobin that may bind hydrogen sulfide produced by two of the worm’s symbionts; and (iii) the expression of a very abundant protein for oxygen storage, hemerythrin, that could provide oxygen to the symbionts and the host under anoxic conditions. Additionally, we identified a large repertoire of proteins involved in interactions between the worm's innate immune system and its symbiotic microbiota, such as peptidoglycan recognition proteins, lectins, fibrinogen-related proteins, Toll and scavenger receptors, and antimicrobial proteins.ConclusionsWe show how this worm, over the course of evolutionary time, has modified widely-used proteins and changed their expression patterns in adaptation to its symbiotic lifestyle and describe expressed components of the innate immune system in a marine oligochaete. Our results provide further support for the recent realization that animals have evolved within the context of their associations with microbes and that their adaptive responses to symbiotic microbiota have led to biological innovations.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3293-y) contains supplementary material, which is available to authorized users.

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“…Specifically, mechanisms involved in the interaction between host and symbiont at the cellular and/or molecular level have not been explored. To date, only a few studies have examined related question through microscopic investigations or gene expression (Won et al, 2003;Kádár et al, 2005;Boutet et al, 2011;Bettencourt et al, 2014;Barros et al, 2015). As in other symbioses, B. azoricus may regulate its symbiont population through apoptosis mechanisms or immunological responses.…”

Section: Accepted M Manuscriptmentioning

confidence: 99%

Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus , involvement in symbiosis?

Détrée

Lallier

Tanguy

et al. 2017

Comparative Biochemistry and Physiology Part B: Biochemistry an

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The relationship between the deep-sea mussel Bathymodiolus azoricus and its thiotrophic (SOX) and methanotrophic (MOX) symbionts has been ecologically and functionally well studied.Endosymbiosis is common in deep-sea hydrothermal vent fauna, yet little is known about the molecular mechanisms underlying the regulation of interactions between host and symbionts. In this study we focused on a group of pattern recognition receptors (PRR), called PGRPs that are able to recognize the peptidoglycan of bacterial cell wall. We first characterised the different PGRPs isoforms in B. azoricus gills and identified five paralogs. Among them two displayed a signal peptide. Then, specific probes designed for each paralog were used to perform real-time PCR quantification in gills of individuals showing various bacterial content as a result of in situ experimental procedures. Overall we found a decrease of PGRPs expression when symbionts amount decreases, suggesting an implication of PGRPs in the regulation of symbionts in B. azoricus gills.We therefore hypothesize that secreted proteins could act as cooperation signals to induce colonisation of symbiotic tissue while non-secreted proteins may regulate the density of endosymbionts within the gill tissue.

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Site-related differences in gene expression and bacterial densities in the mussel Bathymodiolus azoricus from the Menez Gwen and Lucky Strike deep-sea hydrothermal vent sites

Cited by 18 publications

References 33 publications

An updated molecular basis for mussel immunity

An updated molecular basis for mussel immunity

Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis

Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus , involvement in symbiosis?

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