The transcriptomic response of the coral <i>Acropora digitifera</i> to a competent <i>Symbiodinium</i> strain: the symbiosome as an arrested early phagosome

Mohamed, Amin R.; Cumbo, Vivian R.; Harii, Saki; Shinzato, Chuya; Chan, Cheong Xin; Ragan, Mark A.; Bourne, David G.; Willis, Bette L.; Ball, Eldon E.; Satoh, Noriyuki; Miller, David J.

doi:10.1111/mec.13659

Cited by 103 publications

(155 citation statements)

References 57 publications

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“…However, a few experiments investigated differential gene expression in coral larvae with and without symbionts, all of which reported the absence of or rather small gene expression differences in the transcriptomes of symbiotic hosts when compared to the aposymbiotic state (deBoer et al, 2007;Voolstra et al, 2009b;Schnitzler and Weis, 2010). Only recently, a study by Mohamed et al (2016) detected a transient period of differential expression involving a limited number of genes (3% of assayed transcriptome) 4 h after the exposure of Acropora digitifera planula larvae to a competent strain of Symbiodinium. While yet to be applied for larval studies, symbiosis-specific genes have been identified recently in Aiptasia anemones (Bucher et al, 2016;Wolfowicz et al, 2016).…”

Section: Biochemical and Molecular Relationshipmentioning

confidence: 99%

“…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%

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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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Section: Biochemical and Molecular Relationshipmentioning

confidence: 99%

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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“…A key antioxidant in the oxidative stress response in symbiotic cnidarians turns out to be glutathione (Sunagawa et al, 2009; Meyer and Weis, 2012). The gene encoding glutathione S-transferase was previously observed to be downregulated in corals, sea anemones, different strains of green hydra and Paramecium (Kodama et al, 2014; Lehnert et al, 2014; Ishikawa et al, 2016; Mohamed et al, 2016). Our study supports this view (Table 1) and may point to a conserved feature of oxidative stress response in algal-animal symbiosis.…”

Section: Resultsmentioning

confidence: 99%

“…Previous studies have suggested that during establishment of coral–algal symbiosis the host immune response may be partially suppressed (Weis et al, 2008; Mohamed et al, 2016). Our observations in Hydra together with previous findings in corals indicate that regulation of symbiosis by innate immunity pathways indeed may be a general feature of cnidarian symbiosis.…”

Section: Resultsmentioning

confidence: 99%

“…Host lectin-algal glycan interactions have been proposed to be involved in infection and recognition of symbionts in some cnidarians including green hydra, sea anemones and corals (Meints and Pardy, 1980; Lin et al, 2000; Wood-Charlson et al, 2006). Interestingly, up-regulation of C-type lectin genes was also observed during onset of cnidarian–dinoflagellate symbiosis (Grasso et al, 2008; Schwarz et al, 2008; Sunagawa et al, 2009; Mohamed et al, 2016). …”

Section: Resultsmentioning

confidence: 99%

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Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis

Hamada

Schröder

Bathia

et al. 2018

eLife

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Many multicellular organisms rely on symbiotic associations for support of metabolic activity, protection, or energy. Understanding the mechanisms involved in controlling such interactions remains a major challenge. In an unbiased approach we identified key players that control the symbiosis between Hydra viridissima and its photosynthetic symbiont Chlorella sp. A99. We discovered significant up-regulation of Hydra genes encoding a phosphate transporter and glutamine synthetase suggesting regulated nutrition supply between host and symbionts. Interestingly, supplementing the medium with glutamine temporarily supports in vitro growth of the otherwise obligate symbiotic Chlorella, indicating loss of autonomy and dependence on the host. Genome sequencing of Chlorella sp. A99 revealed a large number of amino acid transporters and a degenerated nitrate assimilation pathway, presumably as consequence of the adaptation to the host environment. Our observations portray ancient symbiotic interactions as a codependent partnership in which exchange of nutrients appears to be the primary driving force.

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Symbiont type and environmental factors affect transcriptome‐wide gene expression in the coral Montipora capitata

Helmkampf

Bellinger

Frazier

et al. 2018

Ecology and Evolution

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Reef‐building corals may harbor genetically distinct lineages of endosymbiotic dinoflagellates in the genus Symbiodinium, which have been shown to affect important colony properties, including growth rates and resilience against environmental stress. However, the molecular processes underlying these differences are not well understood. In this study, we used whole transcriptome sequencing (RNA‐seq) to assess gene expression differences between 27 samples of the coral Montipora capitata predominantly hosting two different Symbiodinium types in clades C and D. The samples were further characterized by their origin from two field sites on Hawai‘i Island with contrasting environmental conditions. We found that transcriptome‐wide gene expression profiles clearly separated by field site first, and symbiont clade second. With 273 differentially expressed genes (DEGs, 1.3% of all host transcripts), symbiont clade had a measurable effect on host gene expression, but the effect of field site proved almost an order of magnitude higher (1,957 DEGs, 9.6%). According to SNP analysis, we found moderate evidence for host genetic differentiation between field sites (F ST = 0.046) and among corals harboring alternative symbiont clades (F ST = 0.036), suggesting that site‐related gene expression differences are likely due to a combination of local adaptation and acclimatization to environmental factors. The correlation between host gene expression and symbiont clade may be due to several factors, including host genotype or microhabitat selecting for alternative clades, host physiology responding to different symbionts, or direct modulation of host gene expression by Symbiodinium. However, the magnitude of these effects at the level of transcription was unexpectedly small considering the contribution of symbiont type to holobiont phenotype.

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The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome

Cited by 103 publications

References 57 publications

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

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

Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis

Symbiont type and environmental factors affect transcriptome‐wide gene expression in the coral Montipora capitata

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