Molecular analyses of the gill symbiosis of the bathymodiolin mussel Gigantidas platifrons

Wang, Hao; Zhang, Huan; Zhong, Zhaoshan; Sun, Yan; Wang, Minxiao; Chen, Hao; Zhou, Li; Cao, Lei; Lian, Chao; Li, Chaolun

doi:10.1016/j.isci.2020.101894

Cited by 22 publications

(20 citation statements)

References 102 publications

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“…We observed a significant increase in Candidatus Vesicomyosocius in PA (PA relative abundance = 32.8%, NPA relative abundance = 1.63%, p = 0.0079) and Methyloprofundus (PA relative abundance = 16.9%, NPA relative abundance = 1.25%, p = 0.0043). The chemoautotrophic bacteria are considered symbionts that fix carbon dioxide, detoxify hydrogen sulfide, and provide their hosts with organic carbon compounds ( Wang et al, 2021 ). Endosymbiotic relationships with chemosynthetic bacteria have enabled many deep-sea invertebrates to flourish in hydrothermal vents and cold seeps ( Ip et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Effects of scale worm parasitism on interactions between the symbiotic gill microbiome and gene regulation in deep sea mussel hosts

et al. 2022

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Diverse adaptations to the challenging deep sea environment are expected to be found across all deep sea organisms. Scale worms Branchipolynoe pettiboneae are believed to adapt to the deep sea environment by parasitizing deep sea mussels; this biotic interaction is one of most known in the deep sea chemosynthetic ecosystem. However, the mechanisms underlying the effects of scale worm parasitism on hosts are unclear. Previous studies have revealed that the microbiota plays an important role in host adaptability. Here, we compared gill-microbiota, gene expression and host-microorganism interactions in a group of deep sea mussels (Gigantidas haimaensis) parasitized by scale worm (PA group) and a no parasitic control group (NPA group). The symbiotic microorganism diversity of the PA group significantly decreased than NPA group, while the relative abundance of chemoautotrophic symbiotic bacteria that provide the host with organic carbon compounds significantly increased in PA. Interestingly, RNA-seq revealed that G. haimaensis hosts responded to B. pettiboneaei parasitism through significant upregulation of protein and lipid anabolism related genes, and that this parasitism may enhance host mussel nutrient anabolism but inhibit the host’s ability to absorb nutrients, thus potentially helping the parasite obtain nutrients from the host. In an integrated analysis of the interactions between changes in the microbiota and host gene dysregulation, we found an agreement between the microbiota and transcriptomic responses to B. pettiboneaei parasitism. Together, our findings provide new insights into the effects of parasite scale worms on changes in symbiotic bacteria and gene expression in deep sea mussel hosts. We explored the potential role of host-microorganism interactions between scale worms and deep sea mussels, and revealed the mechanisms through which scale worm parasitism affects hosts in deep sea chemosynthetic ecosystem.

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Section: Discussionmentioning

confidence: 99%

Effects of scale worm parasitism on interactions between the symbiotic gill microbiome and gene regulation in deep sea mussel hosts

et al. 2022

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“…Based on the previously reported genome and transcriptome information of G. platifrons , GpTLR13 was greatly expanded and highly expressed in gill tissue, implying its potential role in symbiosis ( Wong et al, 2015 ; Sun et al, 2017 ). Meanwhile, recent study reported that TLRs were significantly enriched in bacteriocyte transcriptomes in G. platifrons by profiling the transcriptomes of the gill, bacteriocyte, and symbiont, respectively, which confirmed the important role of TLRs in symbiosis ( Wang et al, 2021 ). Therefore, the molecular character and immune function of GpTLR13 were further analyzed to address its role in symbiosis.…”

Section: Discussionmentioning

confidence: 67%

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

Chen

Wang

et al. 2021

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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.

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“…The in situ hybridization assay (ISH) was conducted as previously described (50). For the verification of cell types, cell markers were cloned with gene-specific primers to synthesize the digoxigenin labelled ISH probes.…”

Section: Methodsmentioning

confidence: 99%

Single-cell perspectives on the function and development of deep-sea mussel bacteriocytes

Chen

Wang

et al. 2022

Preprint

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Symbiosis is known to be a major force driving the adaptation and evolution of multicellular organisms. The symbiotic cells and organs, on the meantime, directly provide the mutualist services to the host as the source of phenotypic complexity and outcome of development plasticity. The investigations on the formation and development of symbiotic cells and organs however still remain a challenge in both model and non-model holobionts. Here, by constructing the high-resolution single-cell expression atlas of gill tissue, we have thoroughly surveyed the population census and function atlas of bacteriocytes in deep-sea mussel. Results showed that the bacteriocytes have markedly reshaped its metabolism and are highly coordinated with the endosymbionts in the metabolism of sterol, carbohydrate and ammonia. The immune process of bacterioytes is also robustly adjusted to facilitate the recognition, engulfment, elimination and transcellular transport of endosymbionts. Noticeably, we recognized that the molecular function of bacteriocytes could be guided synergistically by co-option of several conserved transcription factors of the regulatory networks. Moreover, these conserved transcription factors were also responsible for the differentiation and maturation of bacteriocyte lineages. Our results have for the first time revealed the coordination in the function and development of deep-sea mussel symbiotic cells, which was mediated by an ancestral and intrinsic toolkit that conserved across mollusk and could be influenced by symbionts. The coordination while greatly improved our knowledge on how deep-sea mussel thrive in the extreme environment of deep-sea, also highlighted a promising roadmap in revealing the formation and development of symbiotic cells and organs in all holobionts.

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Molecular analyses of the gill symbiosis of the bathymodiolin mussel Gigantidas platifrons

Cited by 22 publications

References 102 publications

Effects of scale worm parasitism on interactions between the symbiotic gill microbiome and gene regulation in deep sea mussel hosts

Effects of scale worm parasitism on interactions between the symbiotic gill microbiome and gene regulation in deep sea mussel hosts

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

Single-cell perspectives on the function and development of deep-sea mussel bacteriocytes

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