Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm

Gao, Zhaoming; Xu, Ting; Chen, Hua-Guan; Li, Rui; Tao, Jun; Wang, Hongbin; Qiu, Jian‐Wen; Wang, Yong

doi:10.1016/j.isci.2023.107033

Cited by 1 publication

(4 citation statements)

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“…4 ), underscoring the genus’s ability to form a broad range of associations with bivalves. Catillopecten margaritatus usually lives on the empty shells of vesicomid A. marissinica or the sediment around aggregations of the tubeworm S. annulatum [ 24 ]. Although they co-occur, the SOB symbionts of these three species showed huge phylogenetic divergences [ 5 , 22 , 24 ], which may reflect their distinct evolutionary histories and subtle physiological differences allowing them to exploit sulfur resources in the heterogeneous habitats.…”

Section: Resultsmentioning

confidence: 99%

“…The relative transcriptional levels of these two systems differ among these symbionts, which might be related to their different habitats and material sources. Those SOBs associated with animals capable of obtaining hydrogen sulfide from the sediment tend to show high transcriptional of the rDSR pathway, such as those of the clams A. marissinica [ 5 ] and Solemya velum [ 77 ], and the tubeworms Riftia pachyptila [ 78 ], Paraescarpia echinospica [ 79 ], and S. annulatum [ 24 ]. By contrast, the SOX multienzyme complex, utilizing thiosulfate from ambient water, is more transcriptionally active than rDSR pathway in bathymodioline symbionts [ 7 ].…”

Section: Resultsmentioning

confidence: 99%

“…The thiotrophic symbionts of vesicomyids, bathymodiolines, and siboglinids encode complete dissimilatory nitrate reduction pathways to provide electron accepters and ammonia [ 6 , 24 , 74-76 , 79 ]. Our previous study found that the δ 15 N value of C. margaritatus (9.9‰) was substantially higher than those of clams, mussels, and tubeworms reliant on SOB for nutrients only [ 23 ].…”

Section: Resultsmentioning

confidence: 99%

“…thermophilus ) inhabiting vents encode hydrogenases [ 74 , 86 , 87 ], whereas seep-dwelling clam Thyasira sp. and tubeworm S. annulatum lack these genes [ 6 , 24 ]. In line with this hypothesis, we found that the genome of Ca.…”

Section: Resultsmentioning

confidence: 99%

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Scallop-bacteria symbiosis from the deep sea reveals strong genomic coupling in the absence of cellular integration

Lin,

Ip,

et al. 2024

The ISME Journal

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Previous studies have revealed tight metabolic complementarity between bivalves and their endosymbiotic chemosynthetic bacteria, but little is known about their interactions with ectosymbionts. Our analysis of the ectosymbiosis between a deep-sea scallop (Catillopecten margaritatus) and a gammaproteobacterium showed that bivalves could be highly interdependent with their ectosymbionts as well. Our microscopic observation revealed abundant sulfur-oxidizing bacteria (SOB) on the surfaces of the gill epithelial cells. Microbial 16S rRNA gene amplicon sequencing of the gill tissue showed the dominance of the SOB. An analysis of the SOB genome showed that it is substantially smaller than its free-living relatives and has lost cellular components required for free-living. Genomic and transcriptomic analyses showed that this ectosymbiont relies on rhodanese-like proteins and SOX multienzyme complex for energy generation and mainly on the CBB cycle for carbon assimilation. The symbiont encodes an incomplete TCA cycle that could also assimilate inorganic carbon via a phosphoenolpyruvate carboxylase. Observation of the scallop’s digestive gland and its nitrogen metabolism pathways indicates it does not fully rely on the ectosymbiont for nutrition. Analysis of the host’s gene expression provided evidence that it could offer intermediates for the ectosymbiont to complete its TCA cycle and some amino acid synthesis pathways using exosomes, and its phagosomes, endosomes, and lysosomes might be involved in harvesting nutrients from the symbionts. Overall, our study prompts us to rethink the intimacy between the hosts and ectosymbionts in Bivalvia and the evolution of chemosymbiosis in general.

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