Tenacious D: <i>Symbiodinium</i> in clade D remain in reef corals at both high and low temperature extremes despite impairment

Silverstein, Rachel N.; Cunning, Ross; Baker, Andrew C.

doi:10.1242/jeb.148239

Cited by 107 publications

(108 citation statements)

References 41 publications

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“…The most thermoresistant colony (#3) had constitutively higher NF-κB levels and hosted a variety of Durusdinium symbionts as compared to thermosensitive colonies 1 and 2, which had lower NF-κB levels and hosted primarily Cladocopium symbionts. Several studies have reported that hosting Durusdinium is associated with increased thermotolerance in corals (e.g., Barshis et al, 2013;Silverstein et al, 2017;Gates, 2011, Davies et al, 2018). Whether host factors, such as increased NF-κB levels, also contribute to the bleaching resistance in our P. damicironis colony 3 is not clear at this time.…”

Section: Discussionmentioning

confidence: 99%

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Mansfield¹,

Cleves

Vlack³

et al. 2019

Preprint

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Many cnidarians, including the reef-building corals, undergo symbiotic mutualisms with photosynthetic dinoflagellate algae of the family Symbiodiniaceae. These partnerships are sensitive to temperature extremes, which cause symbiont loss and increased coral mortality.Previous studies have implicated host immunity and specifically immunity transcription factor NF-κB as having a role in the maintenance of the cnidarian-algal symbiosis. Here we have further investigated a possible role for NF-κB in establishment and loss of symbiosis in various strains of the anemone Exaiptasia (Aiptasia) and in the coral Pocillopora damicornis. Our results show that NF-κB expression is reduced in Aiptasia larvae and adults that host certain algae strains. Treatment of Aiptasia larvae with a known symbiosis-promoting cytokine, transforming growth factor β , also led to decreased NF-κB expression. We also show that aposymbiotic Aiptasia (with high NF-κB expression) have increased survival following infection with the pathogenic bacterium Serratia marcescens as compared to symbiotic Aiptasia (low NF-κB expression). Furthermore, a P. damicornis coral colony hosting Durusdinium spp. (formerly clade D) symbionts had higher basal NF-κB expression and decreased heat-induced bleaching as compared to two individuals hosting Cladocopium spp. (formerly clade C) symbionts. Lastly, genome-wide gene expression profiling and genomic promoter analysis identified putative NFκ B target genes that may be involved in thermal bleaching, symbiont maintenance, and/or immune protection in P. damicornis. Our results provide further support for the hypothesis that modulation of NF-κB and immunity plays a role in some, but perhaps not all, cnidarian-Symbiodiniaceae partnerships as well as in resistance to pathogens and bleaching. 2017; Mansfield et al., 2017; Williams et al., 2018). We and others have shown that the expression and activity of NF-κB are modulated during the onset of symbiosis and after loss of symbiosis in both Aiptasia (Wolfowicz et al., 2016; Mansfield et al., 2017) and the coral Acropora palmata (DeSalvo et al., 2010). For example, Mansfield et al. (2017) demonstrated that the establishment of algal symbiosis in naïve Aiptasia larvae is associated with a reduction in NF-κB expression and that heat-induced loss of symbiosis in adult Aiptasia is associated with increased NF-κB expression and DNA-binding activity. Furthermore, genomic analyses have shown that symbiotic cnidarians, such as the coral Pocillopora damicornis (Cunning et al., 2018), have extensive repertoires of immune signaling genes. Based on these data, we hypothesized that algal symbionts can modulate host NF-κB expression to effect a decrease in host immunity to allow for the establishment of symbiosis (Mansfield et al., 2017; Mansfield and Gilmore, 2019).Herein, we have used Aiptasia and P. damicornis to further investigate Symbiodiniaceaeinduced downregulation of NF-κB, as well as the implications of decreased NF-κB levels and symbiont type for cnidarian immunity and suscept...

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Section: Discussionmentioning

confidence: 99%

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Mansfield¹,

Cleves

Vlack³

et al. 2019

Preprint

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“…However, the P. Although partnerships with resistant Symbiodinium clades could afford greater bleaching resistance under extreme heat events (Silverstein, Cunning, & Baker, 2017), such evidence suggests that other factors may influence the conservation of associated and/or dominant symbiont lineages within these colonies. Though the focus of this study was not to assess clade assemblage at such fine resolution, it is important to consider that gradients of clade associations can afford varied environmental tolerances.…”

Section: Dna Isolation Amplification and Symbiont Variation Comparisonmentioning

confidence: 99%

Conservation of Symbiodinium spp. clade in the coral Pocillopora damicornis during the 2014 mass-bleaching event

Murphy

Spies

Richmond

2018

Preprint

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Symbiotic single-celled dinoflagellates play critical roles in providing corals with both energy and tolerances to survive over a range of environmental conditions. Stressors can cause the breakdown of this symbiosis, resulting in mass bleaching events, and are projected to increase in frequency and spatial extent, threatening the long-term survival of coral reefs. Recent studies have identified symbiont shuffling in corals towards more thermo-tolerant clades as a functional tool for their surviving thermally-induced stress events. However, this was not observed within Pocillopora damicornis colonies tracked over a complete bleaching to recovery cycle during the 2014 mass coral bleaching event in Hawai'i. Instead, previously acquired symbiont clades were maintained following bleaching recovery. This observation suggests additional factors may be involved in thermal-stress acclimation and adaptation in this coral. AbstractSymbiotic single-celled dinoflagellates play critical roles in providing corals with both energy and tolerances to survive over a range of environmental conditions. Stressors can cause the breakdown of this symbiosis, resulting in mass bleaching events, and are projected to increase in frequency and spatial extent, threatening the long-term survival of coral reefs. Recent studies have identified symbiont shuffling in corals towards more thermo-tolerant clades as a functional tool for their surviving thermally-induced stress events. However, this was not observed within Pocillopora damicornis colonies tracked over a complete bleaching to recovery cycle during the 2014 mass coral bleaching event in Hawai'i. Instead, previously acquired symbiont clades were maintained following bleaching recovery. This observation suggests additional factors may be involved in thermal-stress acclimation and adaptation in this coral.

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“…Dinoflagellates in the family Symbiodiniaceae reside in the tissues of corals, giant clams, and other marine invertebrates, and have been empirically demonstrated to influence the ability of corals to survive stress events (Baker, 2001; Baker, Starger, McClanahan, & Glynn, 2004; Kenkel & Bay, 2018; Todd C. LaJeunesse et al, 2010; Todd C. LaJeunesse, Smith, Finney, & Oxenford, 2009; Manzello et al, 2018; Rouzé, Lecellier, Saulnier, & Berteaux-Lecellier, 2016). Particular Symbiodiniaceae species, such as Durusdinium trenchii , are more likely to remain associated with hosts and/or to retain photosynthetic function during acute temperature anomalies or extremes (Manzello et al, 2018; Silverstein, Cunning, & Baker, 2015; but see Silverstein et al, 2017). For example, in a dominant reef-building Pacific coral (Acropora millepora) , a Durusdinium species minimized bleaching (a diminished host health state characterized by loss of Symbiodiniaceae en masse) and increased host survival of acute thermal anomalies (Bay, Doyle, Logan, & Berkelmans, 2016; Berkelmans & van Oppen, 2006; A. M. Jones, Berkelmans, van Oppen, Mieog, & Sinclair, 2008; Mieog et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Symbiont community diversity is more constrained in holobionts that tolerate diverse stressors

Howe‐Kerr

Bachelot

Wright³

et al. 2019

Preprint

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AbstractCoral reefs are experiencing global declines as climate change and other stressors cause environmental conditions to exceed the physiological tolerances of host organisms and their microbial symbionts (collectively termed the holobiont). To assess the role of symbiont community composition in holobiont stress tolerance, diversity metrics and abundances of obligate dinoflagellate endosymbionts (Family: Symbiodiniaceae) were quantified from eight Acropora millepora coral colonies (hereafter called genets) that thrived under or responded poorly to various stressors. Four ‘best performer’ coral genets were selected for analysis because they survived 10 days of high temperature, high pCO2, bacterial addition, or combined stressors, whereas four ‘worst performer’ coral genets were analyzed because they experienced significant mortality under these stressors. At the end of the experimental period, seven of eight coral genets mainly hosted Cladocopium symbionts, but also contained Brevolium, Durusdinium, and/or Gerakladinium symbionts at lower abundances (<0.1% of the total community). After 10 days of stress, symbiont communities varied significantly among host genets, but not stress treatments, based on alpha and beta diversity metrics. A generalized joint attribute model (GJAM) also predicted that symbiont communities were primarily sensitive to host genet at regional scales. Indicator species analysis and the regional GJAM model identified significant associations among particular symbionts and host genet performance. Specifically, Cladocopium 3k contributed to the success of best performer host genets under various stressful conditions, whereas Durusdinium glynnii and Durusdinium trenchii were significantly associated with one worst performer genet. Cladocopium 3k dominance should be more broadly investigated as a potential predictor of stress resistance in Acropora millepora populations across their geographic range. Symbiodiniaceae communities exhibited higher richness and variance (beta diversity) in the worst performing genets. These findings highlight that symbiont community diversity metrics may be important indicators of resilience in hosts central to diverse disciplines, from agriculture to medicine.

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Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment

Cited by 107 publications

References 41 publications

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Conservation of Symbiodinium spp. clade in the coral Pocillopora damicornis during the 2014 mass-bleaching event

Symbiont community diversity is more constrained in holobionts that tolerate diverse stressors

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