Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes

Abstract

Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macro benthos such as mussels. But the lack of genome information hinders the understanding of the adaptation of these animals to such inhospitable environments. Here we report the genomes of a deep-sea vent/seep mussel (Bathymodiolus platifrons) and a shallow-water mussel (Modiolus philippinarum). Phylogenetic analysis shows that these mussel species diverged approximately 110.4 million years ago. Many gene families, especially those for stabilizing protein structures and removing toxic substances from cells, are highly expanded in B. platifrons, indicating adaptation to extreme environmental conditions. The innate immune system of B. platifrons is considerably more complex than that of other lophotrochozoan species, including M. philippinarum, with substantial expansion and high expression levels of gene families that are related to immune recognition, endocytosis and caspase-mediated apoptosis in the gill, revealing presumed genetic adaptation of the deep-sea mussel to the presence of its chemoautotrophic endosymbionts. A follow-up metaproteomic analysis of the gill of B. platifrons shows methanotrophy, assimilatory sulfate reduction and ammonia metabolic pathways in the symbionts, providing energy and nutrients, which allow the host to thrive. Our study of the genomic composition allowing symbiosis in extremophile molluscs gives wider insights into the mechanisms of symbiosis in other organisms such as deep-sea tubeworms and giant clams.

Chromosome‐level genome assembly of the razor clam Sinonovacula constricta (Lamarck, 1818)

“…High heterozygosity is a common feature in bivalves’ genomes, which results in assembly errors due to SNP and micro‐insertions or microdeletions between heterozygous alleles. The heterozygosity of S. constricta genome was estimated to be 1.55%, which was comparable to that of Bathymodiolus platifrons of 1.24% (Sun et al, ), Modiolus philippinarum of 2.02% (Sun et al, ), Crassostrea gigas (wild) of 1.95% (Zhang et al, ) and Chlamys farreri of 1.77% (Jiao et al, ). In order to solve the high heterozygosity (1.55%) in S. constricta genome assembly, different combinations of parameters had been examined using Purge Haplotigs software (Roach et al, ).…”

“…Similar phenomena have been observed in the genomes of other bivalves. For example, gene families related to “apoptosis” and “immune response” were significantly expanded in C. gigas genome (Zhang et al, ), and gene families associated with “endocytosis” and “apoptosis” were remarkably expanded in B. platifrons genome (Sun et al, ). Those observations might result from the aquatic habitats and filter feeding lifestyle of bivalves, as they must defend themselves against the pathogen invasion via innate immunity.…”

“…Patinopecten yessoensis ) (Wang et al, ) and mussels (i.e. Bathymodiolus platifrons and Modiolus philippinarum ) (Sun et al, ). However, the genome of the razor clam Sinonovacula constricta , a representative organism of most benthic bivalves, has not been determined.…”

Population genetic structure of the deep‐sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific

“…Based on the recognition sites of the BsaXI enzyme, 2b‐RAD tags were extracted from the draft genome of B. platifrons (Sun et al., ), which served as a reference for SNP identification. Alignment of the filtered reads of each individual to the reference was achieved by SOAP v.2.21 (Li et al., ) using the match mode of “find the best hits” (‐M 4), the maximum number of allowed mismatches of two (‐v 2), and no repeat allowed (‐r 0).…”

“…Genomic regions of the identified candidate outlier SNPs were determined by mapping the 2b‐RAD tags that harbored outlier SNPs against the draft genome of B. platifrons (Sun et al., ). For those mapped to the genic regions [i.e., coding DNA sequence (CDS), intron, or 3/5′‐untranslated region (3/5′‐UTR)], their corresponding proteins (i.e., outlier‐associated proteins) and annotations (Sun et al., ) were extracted for functional classification.…”