Host–Endosymbiont Genome Integration in a Deep-Sea Chemosymbiotic Clam

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 co-evolution 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 gigabases, 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 familie, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 megabases 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 co-evolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.

Genomic Signatures Supporting the Symbiosis and Formation of Chitinous Tube in the Deep-Sea Tubeworm Paraescarpia echinospica

“…Given that adult vestimentiferans have lost their digestive system during metamorphosis and rely on endosymbiosis for nutrition, the contraction of GHF families in vestimentiferans might be an adaptation linked to the high reliance on their symbionts for nutrition. The contraction of cellulase genes has been reported in the deep-sea chemosymbiotic clam Archivesica marissinica that has a reduced digestive system ( Ip et al 2021 ). These results indicate that the loss of GHFs is a convergent evolutionary mechanism in chemosymbiotic invertebrates during the shift from phytoplankton-derived to bacteria-based diet.…”

“…Horizontal gene transfer (HGT) from bacteria has been recognized as an important factor modulating genome evolution in a few groups of invertebrates such as nematodes, rotifers, sponges, and endosymbiotic arthropods ( Boto 2014 ; Conaco et al 2016 ; Husnik and McCutcheon 2018 ). Among molluscans, Archivesica marissinica has recently been revealed to contain bacterial genes horizontally transferred from ancestral symbiotic bacteria ( Ip et al 2021 ). However, putative HGT events of bacterial origin have not been investigated in annelids.…”

Genomic insights into the sessile life and biofouling of barnacles (Crustacea: Cirripedia)

“…The homeobox ( Hox ) genes are conserved transcription factors that play crucial roles in the development and segmentation of the anterior–posterior axis in metazoans ( Sun et al., 2019 ; Ip et al., 2021 ). The ancestral arthropod has been hypothesized to possess ten Hox genes (eight with homeotic function and two Hox -like genes) ( Grenier et al., 1997 ).…”

Environment and Diet Influence the Bacterial Microbiome of Ambigolimax valentianus, an Invasive Slug in California

“…In the field, A. valentianus live up to approximately one year [ 52 ], but in a separate laboratory experiment, adult A. valentianus slugs subsisted on the sterile diet for five months before collection [ 76 ], suggesting that (1) the sterile diet provided adequate nutrients or (2) slugs can survive while consuming minimal nutrients. Endosymbionts involved in such relationships with other organisms are within the Proteobacteria phylum [ 77 , 78 , 79 , 80 , 81 ]. Slugs may harbor endosymbionts that aid in the nutrient synthesis critical for their survival.…”