Breakdown of coral colonial form under reduced pH conditions is initiated in polyps and mediated through apoptosis

Abstract

Certain stony corals can alternate between a calcifying colonial form and noncalcifying solitary polyps, supporting the hypothesis that corals have survived through geologic timescale periods of unfavorable calcification conditions. However, the mechanisms enabling this biological plasticity are yet to be identified. Here we show that incubation of two coral species (Pocillopora damicornis and Oculina patagonica) under reduced pH conditions (pH 7.2) simulating past ocean acidification induce tissue-specific apoptosis that leads to the dissociation of polyps from coenosarcs. This in turn leads to the breakdown of the coenosarc and, as a consequence, to loss of coloniality. Our data show that apoptosis is initiated in the polyps and that once dissociation between polyp and coenosarc terminates, apoptosis subsides. After reexposure of the resulting solitary polyps to normal pH (pH 8.2), both coral species regenerated coenosarc tissues and resumed calcification. These results indicate that regulation of coloniality is under the control of the polyp, the basic modular unit of the colony. A mechanistic explanation for several key evolutionarily important phenomena that occurred throughout coral evolution is proposed, including mechanisms that permitted species to survive the third tier of mass extinctions.apoptosis | ocean acidification | corals

Ocean warming and acidification synergistically increase coral mortality

“…1A). In a previous study by Kvitt et al 46,. incubation of two colonial coral species ( Pocillopora damicornis and Oculina patagonica ) at reduced pH induced coenosarc breakdown and loss of coloniality46, suggesting a mechanistic model in which colonial corals rid themselves of energetically costly processes (e.g., calcification, tissue maintenance) through tissue breakdown.…”

“…In a previous study by Kvitt et al 46,. incubation of two colonial coral species ( Pocillopora damicornis and Oculina patagonica ) at reduced pH induced coenosarc breakdown and loss of coloniality46, suggesting a mechanistic model in which colonial corals rid themselves of energetically costly processes (e.g., calcification, tissue maintenance) through tissue breakdown. Long-term exposure to elevated temperatures causes physiological stress to benthic species, such as enhanced respiration47, higher susceptibility to pathogens48, bleaching49, reduced calcification50 and tissue necrosis475051.…”

Molecular and geochemical perspectives on the influence of CO2 on calcification in coral cell cultures

“…Further, cadherin expression was below detection when cells were grown at very high pCO 2 . Disintegration of the coenosarc and separation of polyps has been observed in a related coral, Pocillopora damicornis , in response to acidified growth medium (Kvitt et al ). Therefore, reduction in cell or tissue adhesion appears to be a stress response to increased pCO 2 and may be mediated by cadherin production at moderate pCO 2 , but not at high pCO 2 , and appears unaided by cadherin at very high pCO 2 .…”

“…These include proteins of known function such as the adhesive cadherin and a carbonic anhydrase, as well as poorly characterized highly acidic proteins. Cadherins serve to adhere cells to each other and to substrate (Angst et al ; Kvitt et al ), while carbonic anhydrases interconvert CO 2 and to regulate pH and provide bicarbonate to the calcification reaction (reviewed by Bertucci et al ). Acidic proteins are thought to play several roles in coral calcification from mineral nucleation and growth to termination (Mass et al ).…”

ATP Supply May Contribute to Light-Enhanced Calcification in Corals More Than Abiotic Mechanisms

“…In the end, the prevailing mechanism may be species-specific, however, acidification effects on calcification are unequivocally substantial in the case of sensitive species, even to the point of complete skeleton dissolution in some cases (Kvitt et al, 2015). In our model a stronger abiotic response to external pH could be obtained in two ways: (1) by lowering Ca-ATPase and BAT's transport rates, but this would come at the cost of lowering calcification rates even under normal conditions, which is not compatible with the observation that many reef corals are both sensitive to acidification and have very high growth rates, or (2) by making the paracellular transport pathway more permeable.…”