Acidification increases abundances ofVibrionalesandPlanctomycetiaassociated to a seaweed-grazer system: potential consequences for disease and prey digestion efficiency

Abstract

Ocean acidification significantly affects marine organisms in several ways, with complex interactions. Seaweeds might benefit from rising CO2through increased photosynthesis and carbon acquisition, with subsequent higher growth rates. However, changes in seaweed chemistry due to increased CO2may change the nutritional quality of tissue for grazers. In addition, organisms live in close association with a diverse microbiota, which can also be influenced by environmental changes, with feedback effects. As gut microbiomes are often linked to diet, changes in seaweed characteristics and associated microbiome can affect the gut microbiome of the grazer, with possible fitness consequences. In this study, we experimentally investigated the effects of acidification on the microbiome of the invasive brown seaweedSargassum muticumand a native isopod consumerSynisoma nadejda. Both were exposed to ambient CO2conditions (380 ppm, pH 8.16) and an acidification treatment (1,000 ppm, pH 7.86) for three weeks. Microbiome diversity and composition were determined using high-throughput sequencing of the variable regions V5-7 of 16S rRNA. We anticipated that as a result of acidification, the seaweed-associated bacterial community would change, leading to further changes in the gut microbiome of grazers. However, no significant effects of elevated CO2on the overall bacterial community structure and composition were revealed in the seaweed. In contrast, significant changes were observed in the bacterial community of the grazer gut. Although the bacterial community ofS. muticumas whole did not change,OceanospirillalesandVibrionales(mainlyPseudoalteromonas) significantly increased their abundance in acidified conditions. The former, which uses organic matter compounds as its main source, may have opportunistically taken advantage of the possible increase of the C/N ratio in the seaweed under acidified conditions.Pseudoalteromonas,commonly associated to diseased seaweeds, suggesting that acidification may facilitate opportunistic/pathogenic bacteria. In the gut ofS. nadejda,the bacterial genusPlanctomycetiaincreased abundance under elevated CO2. This shift might be associated to changes in food (S. muticum) quality under acidification.Planctomycetiaare slow-acting decomposers of algal polymers that could be providing the isopod with an elevated algal digestion and availability of inorganic compounds to compensate the shifted C/N ratio under acidification in their food.In conclusion, our results indicate that even after only three weeks of acidified conditions, bacterial communities associated to ungrazed seaweed and to an isopod grazer show specific, differential shifts in associated bacterial community. These have potential consequences for seaweed health (as shown in corals) and isopod food digestion. The observed changes in the gut microbiome of the grazer seem to reflect changes in the seaweed chemistry rather than its microbial composition.