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

Metabolite exchange is fundamental to the viability of the cnidarian–Symbiodiniaceae symbiosis and survival of coral reefs. Coral holobiont tolerance to environmental change might be achieved through changes in Symbiodiniaceae species composition, but differences in the metabolites supplied by different Symbiodiniaceae species could influence holobiont fitness. Using 13C stable-isotope labelling coupled to gas chromatography–mass spectrometry, we characterized newly fixed carbon fate in the model cnidarian Exaiptasia pallida (Aiptasia) when experimentally colonized with either native Breviolum minutum or non-native Durusdinium trenchii. Relative to anemones containing B. minutum, D. trenchii-colonized hosts exhibited a 4.5-fold reduction in 13C-labelled glucose and reduced abundance and diversity of 13C-labelled carbohydrates and lipogenesis precursors, indicating symbiont species-specific modifications to carbohydrate availability and lipid storage. Mapping carbon fate also revealed significant alterations to host molecular signalling pathways. In particular, D. trenchii-colonized hosts exhibited a 40-fold reduction in 13C-labelled scyllo-inositol, a potential interpartner signalling molecule in symbiosis specificity. 13C-labelling also highlighted differential antioxidant- and ammonium-producing pathway activities, suggesting physiological responses to different symbiont species. Such differences in symbiont metabolite contribution and host utilization may limit the proliferation of stress-driven symbioses; this contributes valuable information towards future scenarios that select in favour of less-competent symbionts in response to environmental change.

• Publication year

  2018

• Venue

  Proceedings of the Royal Society B

• Publication date

  2018-11-28

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1098/rspb.2018.2336PMID 30487315PMCID PMC6283946
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• 13C labelling revealed differential antioxidant- and ammonium-producing pathway activities between the two symbiont states, consistent with symbiont species-specific physiological responses in the holobiont.

  Confidence 0.91

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• Durusdinium trenchii-colonized hosts exhibited a 40-fold reduction in 13C-labelled scyllo-inositol, pointing to altered interpartner signaling-associated metabolite availability.

  Confidence 0.96

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• Durusdinium trenchii-colonized hosts showed reduced abundance and diversity of 13C-labelled carbohydrates and lipogenesis precursors, indicating altered carbon allocation to host storage metabolism.

  Confidence 0.94

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• Colonization with Durusdinium trenchii was associated with a 4.5-fold reduction in 13C-labelled glucose relative to Breviolum minutum-colonized anemones.

  Confidence 0.98

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review

• 13c stable-isotope labelling

  method

  An isotope-tracing approach that uses 13C enrichment to follow newly fixed carbon into downstream metabolites.

  Aliases: 13C labeling, 13C labelling

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• ammonium-producing pathway

  pathway

  A host-associated metabolic pathway category inferred from labeled-carbon incorporation into ammonium-related metabolism.

  Aliases: ammonium-producing pathways

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• breviolum minutum

  organism, symbiont species

  The native Symbiodiniaceae symbiont species used as one colonizing partner in the host experiments.

  Aliases: B. minutum

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• durusdinium trenchii

  organism, symbiont species

  The non-native Symbiodiniaceae symbiont species used as the alternative colonizing partner in the host experiments.

  Aliases: D. trenchii

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• exaiptasia pallida (aiptasia)

  organism

  The model cnidarian host used to study symbiosis with dinoflagellate symbionts.

  Aliases: Aiptasia

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• gas chromatography–mass spectrometry

  method

  An analytical platform used to separate and detect metabolite species in the labeled samples.

  Aliases: GC-MS

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review
• scyllo-inositol

  metabolite

  An inositol stereoisomer measured among the labeled host metabolites.

  Aliases: 13C-labelled scyllo-inositol

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewKiller Whale (322360f1c1) reviewB (s683577b42) reviewq (76h6bfydm6) reviewAK (4715169a40) reviewAnonymous (12632b8b5f) review

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