Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis

Matthews, Jennifer L.; Oakley, Clinton A.; Lutz, Adrian; Hillyer, Katie E.; Roessner, Ute; Grossman, Arthur R.; Weis, Virginia M.; Davy, Simon K.

doi:10.1098/rspb.2018.2336

Cited by 88 publications

(132 citation statements)

References 85 publications

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“…Furthermore, three Durusdinium isolates populate adult Aiptasia at a reduced level as compared to symbionts SSB01 and SSA01 ( Fig. 2B; Matthews et al, 2018), and in no case did we find that Durusdinium sp. downregulated NF-κB.…”

Section: Discussionmentioning

confidence: 68%

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: 68%

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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“…ARA is an essential polyunsaturated fatty acid (PUFA) that could be acquired by host anemones via translocated photosynthate from their Symbiodiniaceae community, heterotrophic prey capture, or via waste by-products from clownfish symbionts (e.g. [45][46][47][48]). Predicted cytochrome P450 monooxygenase pathways, which catalyse ARA and other PUFAs to biologically active, intercellular signalling molecules (eicosanoids), were also highly variable and enriched primarily in host anemones (figure 2d).…”

Section: Resultsmentioning

confidence: 99%

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

et al. 2020

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All eukaryotic life engages in symbioses with a diverse community of bacteria that are essential for performing basic life functions. In many cases, eukaryotic organisms form additional symbioses with other macroscopic eukaryotes. The tightly linked physical interactions that characterize many macroscopic symbioses create opportunities for microbial transfer, which likely affects the diversity and function of individual microbiomes, and may ultimately lead to microbiome convergence between distantly related taxa. Here, we sequence the microbiomes of five species of clownfish-hosting sea anemones that co-occur on coral reefs in the Maldives. We test the importance of evolutionary history, clownfish symbiont association, and habitat on the taxonomic and predicted functional diversity of the microbiome, and explore signals of microbiome convergence in anemone taxa that have evolved symbioses with clownfishes independently. Our data indicate that host identity and clownfish association shapes the majority of the taxonomic diversity of the clownfish-hosting sea anemone microbiome, and predicted functional microbial diversity analyses demonstrate a convergence among host anemone microbiomes, which reflect increased functional diversity over individuals that do not host clownfishes. Further, we identify upregulated predicted microbial functions that are likely affected by clownfish presence. Taken together our study potentially reveals an even deeper metabolic coupling between clownfishes and their host anemones, and what could be a previously unknown mutualistic benefit to anemones that are symbiotic with clownfishes.

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“…) – of course whether this reflects a response of the bacteria to changing health of (and resource provision by) the Symbiodiniaceae, versus a fundamental change in Symbiodiniaceae fitness as a result of heat stress impacts on the bacteria community, or even an independent temperature effect on both, cannot be resolved from this observation alone. In the case of Symbiodiniaceae and their associated bacteria, resolving ‘who influences who’ is extremely important given that both can potentially influence the emergent properties of cultures, for example, reactive oxygen production and quenching (Vardi et al ., ; Goyen et al ., ), nutrient availability (Croft et al ., ; Suggett et al ., ) and metabolite production (Matthews et al ., ; ). Even so, understanding how Symbiodiniaceae associated bacterial communities change with thermal stress is the first step in uncoupling their functional relationship.…”

Section: Discussionmentioning

confidence: 99%

“…Symbiodiniaceae species may begin to redirect photosynthetic reductants and metabolites towards repairing heat stress‐induced damage (e.g. Matthews et al ., ); in which case the supply of carbon (or other resources) to the heterotrophic bacteria will likely shift in both quantity and composition (Buchan et al ., ), as is observed with other marine phytoplankton as their physiological state changes (Bjørrisen, ; Biddanda and Benner, ). Adjustments to the resource landscape of the microlalgal culture may in turn change the optimal niche for certain bacterial community members to thrive and consequently proliferate.…”

Section: Discussionmentioning

confidence: 99%

Revealing changes in the microbiome of Symbiodiniaceae under thermal stress

Camp

Kahlke

Nitschke

et al. 2020

Environmental Microbiology

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Summary Symbiodiniaceae are a diverse family of marine dinoflagellates, well known as coral endosymbionts. Isolation and in vitro culture of Symbiodiniaceae strains for physiological studies is a widely adopted tool, especially in the context of understanding how environmental stress perturbs Symbiodiniaceae cell functioning. While the bacterial microbiomes of corals often correlate with coral health, the bacterial communities co‐cultured with Symbiodiniaceae isolates have been largely overlooked, despite the potential of bacteria to significantly influence the emergent physiological properties of Symbiodiniaceae cultures. We examined the physiological response to heat stress by Symbiodiniaceae isolates (spanning three genera) with well‐described thermal tolerances, and combined these observations with matched changes in bacterial composition and abundance through 16S rRNA metabarcoding. Under thermal stress, there were Symbiodiniaceae strain‐specific changes in maximum quantum yield of photosystem II (proxy for health) and growth rates that were accompanied by changes in the relative abundance of multiple Symbiodiniaceae‐specific bacteria. However, there were no Symbiodiniaceae‐independent signatures of bacterial community reorganisation under heat stress. Notably, the thermally tolerant Durusdinium trenchii (ITS2 major profile D1a) had the most stable bacterial community under heat stress. Ultimately, this study highlights the complexity of Symbiodiniaceae‐bacteria interactions and provides a first step towards uncoupling their relative contributions towards Symbiodiniaceae physiological functioning.

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Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis

Cited by 88 publications

References 85 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

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

Revealing changes in the microbiome of Symbiodiniaceae under thermal stress

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