Effects of temperature on gene expression in embryos of the coral Montastraea faveolata

Voolstra, Christian R.; Schnetzer, Julia; Peshkin, Leonid; Randall, Carly J.; Szmant, Alina M.; Medina, Mónica

doi:10.1186/1471-2164-10-627

Cited by 132 publications

(169 citation statements)

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“…In addition, it is worthwhile to investigate in the future the impairment of Ca 2+ release as a part of the overall suppression of exocytosis and apoptosis in corals (17,43,44), as Ca 2+ is known signal for apoptosis initiation.…”

Section: Discussionmentioning

confidence: 99%

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Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals

Tchernov

Kvitt

Haramaty

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

183

182

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During the past several decades, numerous reports from disparate geographical areas have documented an increased frequency of "bleaching" in reef-forming corals. The phenomenon, triggered by increased sea surface temperatures, occurs when the cnidarian hosts digest and/or expel their intracellular, photosynthetic dinoflagellate symbionts ("zooxanthellae" in the genus Symbiodinium). Although coral bleaching is often followed by the death of the animal hosts, in some cases, the animal survives and can be repopulated with viable zooxanthellae. The physiological factors determining the ability of the coral to survive bleaching events are poorly understood. In this study, we experimentally established that bleaching and death of the host animal involve a caspase-mediated apoptotic cascade induced by reactive oxygen species produced primarily by the algal symbionts. In addition, we demonstrate that, although some corals naturally suppress caspase activity and significantly reduce caspase concentration under high temperatures as a mechanism to prevent colony death from apoptosis, even sensitive corals can be prevented from dying by application of exogenous inhibitors of caspases. Our results indicate that variability in response to thermal stress in corals is determined by a four-element, combinatorial genetic matrix intrinsic to the specific symbiotic association. Based on our experimental data, we present a working model in which the phenotypic expression of this symbiont/host relationship places a selective pressure on the symbiotic association. The model predicts the survival of the host animals in which the caspase-mediated apoptotic cascade is down-regulated.

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Section: Discussionmentioning

confidence: 99%

“…Although bleaching is highly correlated with increased temperature and high solar irradiance (6-10), it does not always lead to death of the cnidarian host (11)(12)(13). However, the physiological and molecular mechanisms that lead to death of the cnidarian are not adequately understood (14)(15)(16)(17)(18).…”

mentioning

confidence: 99%

Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals

Tchernov

Kvitt

Haramaty

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

183

182

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“…Especially considering reports that some larvae may digest the symbionts instead of engaging in a symbiotic relationship (Titlyanov et al, 1998;Mies et al, 2017c). The available gene expression studies are inconclusive in regard to whether the observed gene expression changes in coral larvae are specific to the symbiont exposure (deBoer et al, 2007;Voolstra et al, 2009a;Schnitzler and Weis, 2010;Mohamed et al, 2016). For instance, it is unclear if these changes are related to a mutualistic relationship or to the mere presence of a foreign algal body.…”

Section: Is There a Mutualism From The Start?mentioning

confidence: 99%

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

et al. 2017

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Symbiodinium are dinoflagellate photosynthetic algae that associate with a diverse array of marine invertebrates, and these relationships are comprehensively documented for adult animal hosts. Conversely, comparatively little is known about the associations during larval development of animal hosts, although four different metazoan phyla (Porifera, Cnidaria, Acoelomorpha, and Mollusca) produce larvae associated with Symbiodinium. These phyla represent considerable diversities in larval forms, manner of symbiont acquisition, and requirements on the presence of symbionts for successful metamorphosis. Importantly, the different requirements are conveyed by specific symbiont types that are selected by the host animal larvae. Nevertheless, it remains to be determined whether these associations during larval stages already represent mutualistic interactions, as evident from the relationship of Symbiodinium with their adult animal hosts. For instance, molecular studies suggest that the host larval transcriptome is nearly unaltered after symbiont acquisition. Even so, a symbiosis-specific gene has been identified in Symbiodinium that is expressed in larval host stages, and similar genes are currently being described for host organisms. However, some reports suggest that the metabolic exchange between host larvae and Symbiodinium may not cover the energetic requirements of the host. Here, we review current studies to summarize what is known about the association between metazoan larvae and Symbiodinium. In particular, our aim was to gather in how far the mutualistic relationship present between adult animals hosts and Symbiodinium is already laid out at the time of symbiont acquisition by host larvae. We conclude that the mutualistic relationship between animal hosts and algal symbionts in many cases is not set up during larval development. Furthermore, symbiont identity may influence whether a mutualism can be established during host larval stages.

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“…More recently, several studies have used gene expression approa ches to detect responses at a molecular level of both coral embryos and larvae subjected to elevated temperatures (e.g. Rodriguez-Lanetty et al 2009, Voolstra et. al 2009, Polato et al 2010, Portune et al 2010.…”

Section: Introductionmentioning

confidence: 99%

Effects of thermal stress on early developmental stages of a gorgonian coral

Kipson¹,

Linares²,

Teixidó³

et al. 2012

Mar. Ecol. Prog. Ser.

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Ongoing sea temperature increase threatens reefs worldwide. In this study we experimentally examined for the first time the response of the early life stages of a long-lived structural gorgonian, the Mediterranean species Paramuricea clavata (Risso 1826), to the highest summer temperature recorded so far in the study area (25°C; the Medes Islands, Northwestern Mediterranean). This temperature also simulates the end-of-century predicted warming (+ 3°C) over the temperature maxima recorded during the species' reproductive period. The results showed a severe negative impact of constant thermal stress on the viability of P. clavata embryos and larvae, resulting in reduced survivorship, completely abnormal embryonic development and impaired metamorphosis. The deteriorating effect was rapid for embryos (after 7 h), whereas the impact on larvae became evident after 10 d of stress. Larval modifications started 7 d earlier under elevated temperature conditions, but the appearance of spherical, aberrant shapes prevented an assessment of whether metamorphosis was initiated but abnormal, or deterred altogether. The apparent higher sensitivity of embryos suggests that thermal stress during embryonic development may be the most critical factor for the viability of P. clavata larvae. In the context of an ongoing warming trend, the reduced viability of early life stages would jeopardize the persistence of P. clavata, which relies on successful recruitment for replenishment of its populations. Further research into the effects of thermal stress on the reproduction of structural invertebrate species and the viability of their early life stages will improve our understanding of the long-term consequences of environmental global change in marine benthic communities.KEY WORDS: Temperature stress · Octocoral · Embryogenesis · Larval development · Mediterranean Sea · Global warming Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 470: [69][70][71][72][73][74][75][76][77][78] 2012 elevated temperature on tropical or subtropical scleractinian corals, while data on octocorals and temperate corals are lacking (but see Zeevi-Ben-Yosef & Benayahu 2008).The Mediterranean region is considered to be among the main climate change hotspots (Giorgi 2006), where several mass mortality events of invertebrates, caused by positive seawater temperature anomalies, were recently observed ). During the 2 largest mass mortality events recorded to date (in 1999 and 2003), both in terms of the range of species affected (~30 species from 5 phyla) and the geographic extent (~1000 km of coastline), temperatures reached ~3 to 4°C above average (Cerrano et al. 2000, Crisci et al. 2011. These large events were accompanied by several others, affecting fewer species or being more localized, e.g. in summers of (Bensoussan et al. 2010, Maldonado et al. 2010, Cebrian et al. 2011, Huete-Stauffer et al. 2011, Stabili et al. 2012. In general, gorgonians, which are structurally important elements of Mediterranean...

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Effects of temperature on gene expression in embryos of the coral Montastraea faveolata

Cited by 132 publications

References 45 publications

Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals

Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

Effects of thermal stress on early developmental stages of a gorgonian coral

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