Functional stability of Spirochaetota symbionts in the precious octocoral Corallium rubrum under heat stress.

Abstract

Background: Octocoral gorgonians are the engineer species of the Mediterranean coralligenous assemblages, but they are threatened with collapse due to recurring marine heat waves. These extreme events disrupt their symbiotic relationship with their associated microbes, promoting pathogen proliferation and tissue-degrading diseases. While the effects of seawater warming on microbial taxonomic diversity have been extensively studied, the functional response of bacterial symbionts and opportunists to thermal stress in Mediterranean octocorals has not yet been investigated. To fill this gap, we investigated a unique and very stable symbiosis between the emblematic red coral Corallium rubrum and its Spirochaetota symbionts. Although the relative and absolute abundances of Spirochaetota are not affected by heat stress, these symbionts may lose their functions within the coral holobiont.

Results: Our results infer that the Spirochaetota bacterial symbionts of C. rubrum underwent only limited functional changes in response to thermal stress, consistent with their stable abundance in coral tissue. These symbionts may play a role in enhancing the tolerance of C. rubrum to temperature fluctuations by maintaining essential amino acid and vitamin biosynthesis. However, thermal stress affected other groups of bacteria, with Gammaproteobacteria showing reduced functionality (with the exception of Vibrionales, which may contribute to the deterioration of coral health) and Alphaproteobacteria showing increased opportunistic activity. In addition, many differentially expressed genes were associated with the sulfur cycle, highlighting its key role in shaping coral-associated bacterial communities under thermal stress.

Conclusions: The stability of the bacterial symbionts of C. rubrum, especially Spirochaetota, despite thermal stress, is consistent with their constant presence in octocoral tissues. These symbionts contribute to coral resilience by maintaining essential biosynthetic processes. However, the increased activity of opportunistic and pathogenic bacteria such as Vibrio suggests that C. rubrum may be susceptible to the recurring heat waves of the summer season.