Microbiome diversity and host immune functions may define the fate of sponge holobionts under future ocean conditions

Abstract

The sponge-associated microbial community contributes to the overall health and adaptive capacity of the sponge holobiont. This community is regulated by the environment, as well as the immune system of the host. However, little is known about the effect of environmental stress on the regulation of host immune functions and how this may, in turn, affect sponge-microbe interactions. In this study, we compared the microbiomes and immune repertoire of two sponge species, the demosponge, Neopetrosia compacta and the calcareous sponge, Leucetta chagosensis, under varying levels of acidification and warming stress. Neopetrosia compacta harbors a diverse bacterial assemblage and possesses a rich repertoire of scavenger receptors while L. chagosensis has a less diverse microbiome and an expanded range of pattern recognition receptors and proteins with immunological domains. Upon exposure to warming and acidification, the microbiome and host transcriptome of N. compacta remained stable, which correlated with high survival. In contrast, the bacterial community of L. chagosensis exhibited drastic restructuring and widespread downregulation of host immune-related pathways, which accompanied tissue necrosis and mortality. Differences in microbiome diversity and immunological repertoire of diverse sponge groups highlight the central role of host-microbe interactions in predicting the fate of sponges under future ocean conditions.