Holobiont responses of mesophotic precious red coral Corallium rubrum to thermal anomalies

Abstract

Marine heat waves (MHWs) have increased in frequency and intensity worldwide, causing mass mortality of benthic organisms and loss of biodiversity in shallow waters. The Mediterranean Sea is no exception, with shallow populations of habitat-forming octocorals facing the threat of local extinction. The mesophotic zone, which is less affected by MHWs, may be of ecological importance in conservation strategies for these species. However, our understanding of the response of mesophotic octocoral holobionts to changes in seawater temperature remains limited. To address this knowledge gap, we conducted a study on an iconic Mediterranean octocoral, the red coral Corallium rubrum sampled at 60 m depth and 15 °C. We exposed the colonies to temperatures they occasionally experience (18 °C) and temperatures that could occur at the end of the century if global warming continues (21 °C). We also tested their response to extremely cold and warm temperatures (12 °C and 24 °C). Our results show a high tolerance of C. rubrum to a two-month long exposure to temperatures ranging from 12 to 21 °C as no colony showed signs of tissue loss, reduced feeding ability, stress-induced gene expression, or disruption of host-bacterial symbioses. At 24 °C, however, we measured a sharp decrease in the relative abundance of Spirochaetaceae, which are the predominant bacterial symbionts under healthy conditions, along with a relative increase in Vibrionaceae. Tissue loss and overexpression of the tumor necrosis factor receptor 1 gene were also observed after two weeks of exposure. In light of ongoing global warming, our study helps predict the consequences of MHWs on mesophotic coralligenous reefs and the biodiversity that depends on them.

Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens

“…This is in agreement with previous observations of a decrease in the relative abundance of the dominant bacteria in the microbiome of heat-stressed corals [ 62 , 91 , 97 , 102 ]. However, this pattern is not always associated with tissue loss, as evidenced in recent studies of [ 90 , 91 ] and Corinaldesi et al [ 13 ] on Mediterranean octocorals. This inconsistency is maybe due to the fact that the relative quantification of the symbionts does not accurately reflect actual changes occurring within the microbiota [ 16 , 28 ], and the quantification of the absolute abundance of symbionts is necessary to understand microbial dynamics.…”

“…While temperatures above 24 °C had never been measured at 30 m depth before 2022 and only on a maximum of 4 days per year at 15 m depth (in 2009 and 2012), the year 2022 showed 3 and 10 days with temperatures above 24 °C at 30 and 15 m depth, respectively, indicating that the water column warmed for the first time on record down to 30 m depth in Marseille. Laboratory experiments have identified a temperature of 23–24 °C as a thermal threshold for many Mediterranean octocoral species, above which tissue loss and mortality have been observed [ 10 , 34 , 72 , 90 , 91 , 93 ]. Thus, after several months (from May to September 2022) of exposure to MHWs, many octocoral colonies showed impaired health and tissue loss throughout the Northwestern Mediterranean Sea [ 23 , 32 ].…”

“…In colonies with 90% tissue loss, we observed a significant increase in bacterial diversity, which is likely attributed to the proliferation of opportunistic bacteria. The shift towards a more diverse bacterial community is a commonly observed phenomenon in heat-stressed organisms [ 20 , 82 , 87 , 90 , 91 ], including octocorals and may be a consequence of the temperature-induced changes in the bacterial growth dynamics and/or the octocoral loss of control over the microbiota [ 38 , 49 , 82 ]. Among the opportunistic bacteria, Vibrio sp.…”

“…Disturbances such as heat stress can induce changes in the octocoral microbiota by exerting a downward pressure on the survival of beneficial symbionts, thereby affecting the stress tolerance of the host, and promoting temperature-dependent bacterial diseases. However, there is currently limited research available on the response of the microbiome of Mediterranean octocorals to temperature anomalies representative of MHWs, and none of these studies can explain the extended mortality and tissue loss of octocorals observed during the 2022 MHWs [ 13 , 90 , 91 ]. They reported different responses depending on the octocoral species, sampling depth and colony, with no clear relationship between tissue loss, thermal stress intensity, and microbiome changes.…”

“…They reported different responses depending on the octocoral species, sampling depth and colony, with no clear relationship between tissue loss, thermal stress intensity, and microbiome changes. In the laboratory experiments of Tignat-Perrier et al [ 90 , 91 ], decreases in the relative abundance of the major symbionts ( Endozoicomonas or Spirochaetaceae ) following heat stress (24 °C for several weeks) were associated with tissue loss in Paramuricea clavata , but not in Eunicella cavolini or Corallium rubrum . These findings were partially consistent with in situ data from gorgonian and red coral colonies during the 2011 MHWs [ 13 ], where it was observed that deep colonies of C. rubrum (70 m) exposed to heat stress also had a lower relative abundance of the main symbiont Spirochaetaceae .…”