Adaptations To Deep-sea,Insights From Omic Studies On Bathymodiolus Platifrons

The deep-sea has been considered as a biological desert for marine animals due to its harsh conditions including complete darkness,low temperature and oligotrophic conditions.However,with more and more investigation of deap-sea,it is found that there are numerous flourished ecosystems scattered all around the deap-sea and called as deap-sea chemosythetic ecosystems,which are powered by chemosynthetic bacteria.Over past decades,the topic about how these species adapt to such “hash” habitats has drawn continuous attentions,but remains as an open question.Genome sequencing is a powerful method to study none-model species,and the knowledge of genome size is an important prerequisite.Mussels of subfamily Bathymodiolinae have been found to be one of the dominant species in diverse chemosynthetic ecosystems,among them,Bathymodiolus platifrons has been found to be common in the West-pacfic Ocean.Based on the genome size investigation of a wide range of invertebrates in sampling area,and considering the ecological importance,we choose B.platifrons as model species to study the adaptation to deep-sea.In order to identify the linaege-specific adaptive characteristics of B.platifrons,we conducted genome sequencing and RNAseq of the mussel in a comparative frame with its costal relative Modiolus kurilensis.Compared with coastal mussels,one of the most extraordinary traits of Bathymodiolus mussels is their endosymbiosis.Based on the multi-omic analysis,we also disscussed the interaction relationship of this symbiotic system.Besides,there are debates about the origin of deep-sea life all these years.We also explored the phylogenetic interactions of mussels based on mitochondrial genomes sequencing and analysis,trying to understand the evolutionary transmission of the taxa.Meanwhile,we compared 20 complete mitogenomes of B.platifrons from a vent and a seep to explore the population connectivity.The main results are as follows: 1.Genome size and featuresThe genome size of B.platifrons was about 2.4 Gb and 2.2 Gb estimated by flow cytometry and genome survey respectively.Compared with other genomes of Lophotrochozoa species,the transposon elements were expanded in B.platifrons,especially the helitron elements,which could induce changes in genome,so it might play a role in the genomic rearrangement during the evolution.In addition,the numbers and length of introns in three mussels were higher than those in other mollusks,with the increasing of numbers of alternative splicing,these might be the special features shared in mussels.2.AdaptionsBoth the deep-sea Bathymodiolus mussels and costal mussels possess diverse gene families related to stress responses,there were no specific or significantly expanded families in Bathymodiolus mussels,indicating that all mussels might possess the potential to cope with diverse stresses,but prefering different gene members of the same gene family in different species.Compared with coastal relatives,the symbiotic relationship in deep-sea mussels are one of the most obvious and important difference.From the genomic insight,many gene families related to endocytosis,transporters,glycosylation were expanded or positively selected in deep-sea mussels,which indicated that the symbiotic relationship might have be a selective driver for the evolution of B.platifrons.In deep-sea chemosynthetic ecosystems,many symbiotic invertebrates rely on the chemoautotrophic bacteria for nutrients,with the reduction of their digestive systems.We compared the number of digestion-related genes and expression pattern of different tissues between B.platifrons with other mollusks,the results indicated that B.platifrons mussels still have the potential of digestion,which might be good for the mussels to live in more diverse habitats and adapt to the unstable conditions.3.The origin of deep-sea musselsCombining evidence of the shallow divergence(37.4 Mya),the tip positioning in the phylogenetic trees as well as published fossil records,a recent invasion no older than the mid-cretaceous of Bathymodiolus spp.from shallow water to the deep-sea chemosynthetic ecosystem was supported.Hence,these deep-sea mussels are not living fossils.4.Interactions between B.platifrons and its symbiontsBased on the comparative transcriptomic analysis,we identified several candidate pattern recognition receptors(PRRs)such as TLRs,C1 qDC proteins,which might play a role in host-symbiont recognition.However,the results of statistics of representative PRR numbers using either genomic data or RNA-seq data all indicated that PRRs seemed to be globally reduced in B.platifrons,which might facilitate the infection and maintenance of their symbionts.Phagocytosis or endocytosis might be the routes for their entrance,after that,the symbionts were restricted in host-dedrived membrane and dwelled in host cell.Our results highlighted the lysosomal activities in deep-sea mussels,indicating that nutrients might be absorbed from the symbionts by cellular digestion.Meanwhile,diverse transporters were also identified to be positively selected or more highly expressed in the deep-sea mussels,which could provide more effective exchange of nutrients and intermediate metabolites.To maintain a sustainale symbiotic relationship between Bathymodiolus mussels and their symbionts,related physiological processes such as lysosome activity,autophagy and apoptosis are need to be regulated coordinately,but the mechanisms remains unclear.5.Population connectivityAccording to the genome sequencing and analysis,the two genomes of B.platifrons from the studied hydrothermal vent and cold seep were highly similar.Besides,even with our hypervariable molecular marker,no structured genetic differentiation can be detected for B.platifrons from the seep and vent.The two populations were well connected,possibly by a strong Kuroshio Current during prolonged planktonic larvae stages.