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-insu cient environmentsby harboring sulfur-oxidizing bacteria (SOB)and/or methaneoxidizing 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 sortingassociated proteinwere modulated simultaneously, contributing to the ne tuning of cellular homeostasis, lysosome activity and bacteria engulfment in either symbiotic and nonsymbiotic bacteria challenge.A total of 459 miRNAs were identi ed 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.

Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis

“…Pattern recognition receptors (PRRs) are important for immune recognition and response ( Byeon et al, 2015 ; Graça, 2015 ). Previous studies have reported high levels of PRRs in the symbiotic gill tissue of bathymodiolines, such as G. platifrons , B. septemdierum , and B. azoricus ( Bettencourt et al, 2014 ; Chen et al, 2021 ; Ikuta et al, 2019 ; Li et al, 2020 ; Wang et al, 2019 ), suggesting their importance in symbiosis. Both TLRs and PGRPs have been suggested to participate in endosymbiont establishment and symbiosis regulation ( Li et al, 2021 ; Sun et al, 2017 ).…”

“…C1qs may bind to the surface of pathogens and kill them directly or trigger downstream immune activities ( Jiang et al, 2015 ; Cheng et al, 2019 ). Consequently, C1qs have been suggested to function as scaffolds of PRRs and in symbiont recognition ( Chen et al, 2021 ). Wang et al ( 2021 ) reported high expression of C1qs in the gill tissue of G. platifrons .…”