microRNAs Facilitate Comprehensive Responses of Bathymodiolinae Mussel Against Symbiotic and Nonsymbiotic Bacteria Stimulation

Abstract

Background:As the dominant species inhabiting both cold seeps and hydrothermal vents,Bathymodiolinae mussels are one of the most successful megafauna in the deep sea.They thrive in dark and food-insufficient environmentsby harboring sulfur-oxidizing bacteria (SOB)and/or methane-oxidizing bacteria (MOB)ingill bacteriocytesand obtain the majority of their nutrition from them.Many attempts have been made to decode the mechanisms underlying their symbiosis, which yetremained largely undisclosedfor years due to the lack of cultivable symbionts. In the present study,the globalexpression pattern of immune-related genes and miRNAswere surveyed inGigantidasplatifronsduring bacterial challengesusing enriched symbiontsor nonsymbioticVibrio in attempting to reveal the molecular mechanisms underlying chemosynthetic symbiosis. Results: Multiple PRRs such as TLRs, LRRs and C1q were found vigorously modulated during challenges whiledistinctly clusteredbetween symbiotic and nonsymbiotic bacteria stimulation. As downstream of the immune response,dozens of immune effectors including HSP70, P450, CD82 andvacuolar protein sorting-associated proteinwere modulated simultaneously, contributing to the fine tuning of cellular homeostasis, lysosome activity and bacteria engulfment in either symbiotic and nonsymbiotic bacteria challenge.A total of 459 miRNAs were identified in gill tissue of G. platifrons while dozens of themwere differentially expressedduring the challenge.Among these miRNAs, some were also found in differentexpression patternbetween symbiont or nonsymbiontchallenges and targeting apoptosis and phagosome maturation-related genes, including caspase8, inhibitor of apoptosis, cAMP-responsive element-binding protein,IκB, Rab and integrin. Conclusion:It was suggested that G. platifrons PRRs might function cooperativelyto facilitate the specialized immune recognition to MOBs or nonsymbioticbacteria. Meanwhile, a shared expression pattern of immune effectorswas observed between bacterial challenges, indicatingthe conservative response of Bathymodiolinae mussels in promoting the adhesion andengulfment of symbionts and nonsymbiont. Nevertheless, the differentially expressed miRNAs were yet suggested to facilitate specialized modulationinsymbiosis by repressing apoptosis- and phagosome maturation-related genes.With the orchestra of immune-related genes and miRNAs, G. platifronsmussels could therefore maintain arobust immune response against invading pathogens while establishing symbiosis with chemosynthetic bacteria.

Insights into symbiotic interactions from metatranscriptome analysis of deep‐sea mussel Gigantidas platifrons under long‐term laboratory maintenance

“…Similar results for an activated immune response have been detected in previous analyses of deep‐sea mussels with depleted endosymbionts (Barros et al, 2015; Détrée et al, 2019). Moreover, differential expression of immune‐related genes was also detected in deep‐sea mussels under laboratory acclimation to bacterial challenges of symbiotic and environmental bacteria (Chen, Wang, Zhang, et al, 2021; Wang et al, 2019). Previous studies have revealed a concomitant immune response against symbiont depletion or bacterial invasion, highlighting the importance of immune‐related genes during these processes (Détrée et al, 2017; Wang et al, 2019).…”

“…For example, many critical immune‐related genes have been found to be expanded in the genome of deep‐sea mussels or positively selected in the deep‐sea lineage, revealing their importance in establishing symbiosis (Sun, Zhang, et al, 2017; Zheng et al, 2017). Several reports have demonstrated the participation of some pattern recognition receptors (PRRs), such as toll‐like receptors, C1q domain‐containing proteins, and lectins, in the innate response of Bathymodiolinae mussels to symbiotic and non‐symbiotic bacterial challenges (Chen, Wang, Zhang, et al, 2021; Martins et al, 2015; Wang et al, 2019). As for the nutritional interactions in symbiosis, current studies based on genomic or transcriptomic analysis have reported that various digestive enzymes and transporters might participate in intracellular transport and symbiont digestion and enable the transfer of nutrition from symbionts to the host (Ponnudurai et al, 2017; Zheng et al, 2017).…”