Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts

Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix; Couvillion, Sneha P.; Webster, Nicole; Thomas, Torsten

doi:10.1186/s40168-021-01220-9

Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts

Journal Article · Mon Jan 31 23:00:00 EST 2022 · Microbiome

DOI:https://doi.org/10.1186/s40168-021-01220-9· OSTI ID:1846201

Zhang, Shan ^[1]; Song, Weizhi ^[1]; Nothias, Louis-Félix ^[2]; Couvillion, Sneha P. ^[3]; Webster, Nicole ^[4]; ^[1]

Univ. of New South Wales, Sydney, NSW (Australia)
Univ. of California, San Diego, CA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Australian Institute of Marine Science, Townsville (Australia)

Sponges are ancient sessile metazoans, which form with their associated microbial symbionts a complex functional unit called a holobiont. Sponges are a rich source of chemical diversity; however, there is limited knowledge of which holobiont members produce certain metabolites and how they may contribute to chemical interactions. To address this issue, we applied non-targeted liquid chromatography tandem mass spectrometry (LC-MS/MS) and gas chromatography mass spectrometry (GC-MS) to either whole sponge tissue or fractionated microbial cells from six different, co-occurring sponge species. Several metabolites were commonly found or enriched in whole sponge tissue, supporting the notion that sponge cells produce them. These include 2-methylbutyryl-carnitine, hexanoyl-carnitine and various carbohydrates, which may be potential food sources for microorganisms, as well as the antagonistic compounds hymenialdisine and eicosatrienoic acid methyl ester. Metabolites that were mostly observed or enriched in microbial cells include the antioxidant didodecyl 3,3'-thiodipropionate, the antagonistic compounds docosatetraenoic acid, and immune-suppressor phenylethylamide. This suggests that these compounds are mainly produced by the microbial members in the sponge holobiont, and are potentially either involved in inter-microbial competitions or in defenses against intruding organisms. This study shows how different chemical functionality is compartmentalized between sponge hosts and their microbial symbionts and provides new insights into how chemical interactions underpin the function of sponge holobionts.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; Gordon and Betty Moore Foundation (GBMF)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1846201

Report Number(s):: PNNL-SA--163874

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 10; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Antagonist
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Metabolomics
Sponge
Symbionts

Additional file 2 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106146 The current record is supplemented by this text	text	January 2022
Additional file 2 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106146.v1 The current record is supplemented by this text	text	January 2022
Additional file 3 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106149 The current record is supplemented by this text	text	January 2022
Additional file 3 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106149.v1 The current record is supplemented by this text	text	January 2022
Additional file 4 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106152 The current record is supplemented by this dataset	dataset	January 2022
Additional file 4 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106152.v1 The current record is supplemented by this dataset	dataset	January 2022
Additional file 5 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106155 The current record is supplemented by this dataset	dataset	January 2022
Additional file 5 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106155.v1 The current record is supplemented by this dataset	dataset	January 2022
Additional file 6 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106161 The current record is supplemented by this dataset	dataset	January 2022
Additional file 6 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106161.v1 The current record is supplemented by this dataset	dataset	January 2022
Additional file 7 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106164 The current record is supplemented by this dataset	dataset	January 2022
Additional file 7 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106164.v1 The current record is supplemented by this dataset	dataset	January 2022
Additional file 8 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106167 The current record is supplemented by this dataset	dataset	January 2022
Additional file 8 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106167.v1 The current record is supplemented by this dataset	dataset	January 2022
Additional file 9 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106170 The current record is supplemented by this dataset	dataset	January 2022
Additional file 9 of Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts Zhang, Shan; Song, Weizhi; Nothias, Louis-Félix https://doi.org/10.6084/m9.figshare.19106170.v1 The current record is supplemented by this dataset	dataset	January 2022

Comparative metabolomic analysis reveals shared and unique chemical interactions in sponge holobionts

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