Proteome and Transcriptome Analysis of Gonads Reveals Intersex in Gigantidas haimaensis

Abstract

Sex has proven to be one of the most intriguing areas of research across evolution, development, and ecology. Intersex or sex change occurs frequently in molluscs. The deep-sea mussel Gigantidas haimaensis often dominates within Haima cold seep ecosystems, but details of their reproduction remain unknown. Herein, we conducted a combined proteomic and transcriptomic analysis of G. haimaensis gonads to provide a systematic understanding of sexual development in deep-sea bivalves. A total of 2,452 out of 42,238 genes (5.81%) and 288 out of 7,089 proteins (4.06%) were significantly differentially expressed between ovaries and testes with a false discovery rate (FDR) <0.05. Candidate genes involved in sexual development were identified; among 12 differentially expressed genes between sexes, four ovary-biased genes (β-catenin, fem-1, forkhead box L2 and membrane progestin receptor α) were expressed significantly higher in males than females. Combining histological characteristics, we speculate that the males maybe intersex undergoing sex change, and implied that these genes may be involved in the process of male testis converting into female gonads in G. haimaensis. The results suggest that this adaptation may be based on local environmental factors, sedentary lifestyles, and patchy distribution, and sex change may facilitate adaptation to a changing environment and expansion of the population. The findings provide a valuable genetic resource to better understand the mechanisms of sex change and survival strategies in deep-sea bivalves.

Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals

“…Considering the anatomical observations only, another possibility could have been that the intersex individuals were undergoing sex change (sequential hermaphroditism). For instance, in a recent study of Gigantidas haimaensis mussels from cold seep ecosystems in the South China Sea, Shi et al . (2022) found that male gonads contained oocytes (while female gonads did not contain spermatocytes).…”

“…The copyright holder for this preprint this version posted April 13, 2023. ; https://doi.org/10.1101/2023.04.11.536409 doi: bioRxiv preprint destroy most of the vent communities in a given region (see the recent eruption of the submarine volcano Hunga Tonga -Hunga Ha'apai in December 2021, Gupta et al, 2022). In a recent study of Gigantidas haimaensis mussels from cold seep ecosystems in the South China Sea, Shi et al (2022) found that male gonads contained oocytes (while female gonads did not contain spermatocytes).…”

Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals

“…Considering the anatomical observations only, another possibility could have been that the intersex individuals were undergoing sex change (sequential hermaphroditism). For instance, in a recent study of Gigantidas haimaensis mussels from cold seep ecosystems in the South China Sea, Shi et al (2022) found that male gonads contained oocytes (while female gonads did not contain spermatocytes). Combining proteomic and transcriptomic analyses with their histological observations, the authors hypothesized that these males were intersex individuals undergoing sex change, a strategy observed in other Bathymodiolinae (Laming et al, 2018) possibly favoured by the ephemeral and patchy distribution of deep sea vent and cold seep habitats.…”

Comparative proteomic analysis of cold seep clam Archivesica marissinica and shallow water shellfish Ruditapes philippinarum provides insights into the adaptation mechanisms of deep-sea mollusks

“…These findings suggest the potential utility of these proteins as biomarkers for the evaluation of deep-sea mining endeavors in the future (Kwan et al, 2019). Therefore, proteomics research has been conducted on various marine organisms, including barnacle (Yan et al, 2020), deep-sea mussel (Ponnudurai et al, 2020;Shi et al, 2022), deep sea copepods (Renz et al, 2021), deep sea isopods (Paulus et al, 2022), and so on.…”