Cold adaptation and horizontal gene transfer shape Antarctic sponge microbiomes.

backgroundMarine sponges exhibit wide distribution in tropical, temperate, and polar environments. They host diverse microbiomes important to their survival and ecological roles. Antarctic sponges, thriving in extreme cold environments, harbor unique microbial communities. However, functional differences distinguishing Antarctic sponge microbiomes have been poorly investigated. In this study, we investigated how the functional composition of the microbiomes of Antarctic sponges differs from that of their counterparts in other environments, with a particular focus on functions related to cold adaptation. We also assessed the role of horizontal gene transfer (HGT) in driving these functional adaptations.

resultsAntarctic sponge microbiomes displayed a unique functional signature characterized by significantly higher proportions of genes related to cold adaptation, such as cold shock proteins, chaperones, heat shock proteins, and osmoprotectants, compared to their tropical and temperate counterparts, and antioxidants compared to the surrounding seawater. HGT was prevalent in Antarctic sponge symbionts, particularly in the dominant Gammaproteobacteria, Alphaproteobacteria, and Bacteroidia, contributing equally to metabolic functions and cold adaptation, with an important fraction of the latter exhibiting long-distance horizontal gene transfer (HGT). Conjugation, primarily mediated by integrative and conjugative elements (ICE), is a proposed crucial mechanism driving horizontal gene transfer (HGT) in Antarctic sponge symbionts. The cold shock protein C (CspC), linked to cold adaptation, was restricted to Proteobacteria and identified as a potential horizontally acquired gene exclusive to sponge symbionts compared to free-living bacteria in the Antarctic marine ecosystem.

conclusionsAntarctic sponge microbiomes exhibit higher proportions of functional adaptations for cold environments facilitated by horizontal gene transfer (HGT). These findings highlight the evolutionary importance of HGT mechanisms in shaping microbial symbioses in extreme environments. Further exploration of HGT dynamics and the role of specific symbionts in cold adaptation could reveal novel insights into microbial evolution and host-symbiont interactions in polar ecosystems. Video Abstract.