Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

David Ngugi; Sou Miyake; Matthew Cahill; Manikandan Vinu; Timothy J. Hackmann; Jochen Blom; Matthew Tietbohl; Michael L. Berumen; Ulrich Stingl

doi:10.1073/pnas.1703070114

Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

David Ngugi, Sou Miyake, Matthew Cahill, Manikandan Vinu, Timothy J. Hackmann, Jochen Blom, Matthew Tietbohl, Michael L. Berumen, Ulrich Stingl

Research output: Contribution to journal › Article › peer-review

30 Scopus citations

Abstract

Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown Turbinaria algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage,

Original language	English (US)
Pages (from-to)	E7592-E7601
Number of pages	1
Journal	Proceedings of the National Academy of Sciences
Volume	114
Issue number	36
DOIs	https://doi.org/10.1073/pnas.1703070114
State	Published - Aug 23 2017

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10.1073/pnas.1703070114

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title = "Genomic diversification of giant enteric symbionts reflects host dietary lifestyles",

abstract = "Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown Turbinaria algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage,",

author = "David Ngugi and Sou Miyake and Matthew Cahill and Manikandan Vinu and Hackmann, {Timothy J.} and Jochen Blom and Matthew Tietbohl and Berumen, {Michael L.} and Ulrich Stingl",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank the King Abdullah University of Science and Technology (KAUST) Bioscience Core Lab, the Coastal and Marine Resources Core Lab, and T. Sinclair-Taylor for their technical and logistical support. We also thank John Howard Choat (James Cook University, Queensland) for his insights on surgeonfish nutrition, Andreas Brune (Max Planck Institute for Terrestrial Microbiology, Marburg) for assistance with bacterial nomenclature, and Calder J. Atta (KAUST) for the fish illustrations. This work was supported by KAUST through the Saudi Economic and Development Company Research Excellence Award Program (U.S.).",

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language = "English (US)",

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T1 - Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

AU - Ngugi, David

AU - Miyake, Sou

AU - Cahill, Matthew

AU - Vinu, Manikandan

AU - Hackmann, Timothy J.

AU - Blom, Jochen

AU - Tietbohl, Matthew

AU - Berumen, Michael L.

AU - Stingl, Ulrich

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank the King Abdullah University of Science and Technology (KAUST) Bioscience Core Lab, the Coastal and Marine Resources Core Lab, and T. Sinclair-Taylor for their technical and logistical support. We also thank John Howard Choat (James Cook University, Queensland) for his insights on surgeonfish nutrition, Andreas Brune (Max Planck Institute for Terrestrial Microbiology, Marburg) for assistance with bacterial nomenclature, and Calder J. Atta (KAUST) for the fish illustrations. This work was supported by KAUST through the Saudi Economic and Development Company Research Excellence Award Program (U.S.).

PY - 2017/8/23

Y1 - 2017/8/23

N2 - Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown Turbinaria algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage,

AB - Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown Turbinaria algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage,

UR - http://hdl.handle.net/10754/625748

UR - http://www.pnas.org/content/early/2017/08/22/1703070114.full

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U2 - 10.1073/pnas.1703070114

DO - 10.1073/pnas.1703070114

M3 - Article

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SN - 0027-8424

VL - 114

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JO - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

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ER -

Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

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Gene-centric view of carbohydrate metabolism in quintessential herbivorous fishes from the Red Sea

Epulopiscium Genome sequencing and assembly

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Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

Abstract

UN SDGs

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Gene-centric view of carbohydrate metabolism in quintessential herbivorous fishes from the Red Sea

Epulopiscium Genome sequencing and assembly

Cite this