Long-term effects of ocean acidification and its interaction with warming on calcifying organisms and their associated microbiome: bryozoans as emerging sentinels of global change?

Abstract

Global ocean warming and acidification are two of the major threats to many marine calcifying habitat-forming species, potentially affecting entire ecosystems. Consequently, the need for a better understanding and predicting the response of marine calcifiers has never been more pressing. Paradoxically, the individual and combined long-term effects of these stressors on bryozoans have remained largely unexplored, despite their great abundance and diversity globally. Here, we first evaluate the changes in skeletal structure and mineralogy, and the associated microbiome composition on the populations ofPentapora ottomuelleriana(encrusting) andMyriapora truncata(erect) bryozoan species living inside and outside a volcanic CO2 vent in Ischia Island. We then examine the effects of a long-term exposure to elevated pCO2 and its combined effects of ocean warming on the proportion of cover of populations of the encrusting species through time after summer. Both bryozoan species show indicators of acclimatization by adjusting skeletal properties and having stable microbial communities under acidification conditions. However, we document novel patterns about microbiome shifts in response to future ocean acidification in bryozoans for the first time. Microbial genera known to have essential functions to the host such as biosynthesis of defense compounds or thermal protection were depleted at the acidified site, which suggest early warnings of potential deterioration of bryozoan health under near future ocean conditions. The proportion of cover of the encrusting species also decreased from 2016 to 2020 in both studied sites, with faster declines at the acidified ones. Our model suggests that the increasing seawater temperature drove a decline in the bryozoan cover although the combined effects with acidification accelerated its mortality rates in the CO2 vent. More multidisciplinary research combining both environmental stressors on a wider range of calcifying species is needed to better understand the adaptive capacity of the holobiont to a changing environment.