A multiproducer microbiome generates chemical diversity in the marine sponge Mycale hentscheli
Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microb...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 17; pp. 9508 - 9518 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
28.04.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host Mycale hentscheli in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprisingmicrotubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of M. hentscheli and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential. |
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| AbstractList | Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host
Mycale hentscheli
in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprising microtubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of
M. hentscheli
and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential. Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host Mycale hentscheli in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprising microtubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of M. hentscheli and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential. Bacterial specialized metabolites are increasingly recognized as important factors in animal-microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprising microtubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential. Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host Mycale hentscheli in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprisingmicrotubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of M. hentscheli and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential. Sponges, one of the oldest extant animal phyla, stand out among marine organisms as sources of structurally diverse bioactive natural products. Previous work on chemically rich sponges identified single “superproducer” symbionts in their microbiomes that generate the majority of the bioactive compounds known from their host. Here, we present a contrasting scenario for the New Zealand sponge Mycale hentscheli in which a multiproducer consortium is the basis of chemical diversity. Other than the known cocktail of cytotoxins, metagenomic and functional data support further chemical diversity originating from various uncultivated bacterial lineages. The results provide a rationale for distinct patterns of chemical variation observed within sponge species and reinforce uncultured microbes as promising source of compounds with therapeutic potential. Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host Mycale hentscheli in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprising microtubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of M. hentscheli and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential. |
| Author | Page, Michael J. Field, Christopher M. Rückert, Christian Piel, Jörn Freeman, Michael F. Webb, Victoria L. Kündig, Tomas Rust, Michael Kalinowski, Jörn Sunagawa, Shinichi Nanudorn, Pakjira Helfrich, Eric J. N. |
| Author_xml | – sequence: 1 givenname: Michael surname: Rust fullname: Rust, Michael – sequence: 2 givenname: Eric J. N. surname: Helfrich fullname: Helfrich, Eric J. N. – sequence: 3 givenname: Michael F. surname: Freeman fullname: Freeman, Michael F. – sequence: 4 givenname: Pakjira surname: Nanudorn fullname: Nanudorn, Pakjira – sequence: 5 givenname: Christopher M. surname: Field fullname: Field, Christopher M. – sequence: 6 givenname: Christian surname: Rückert fullname: Rückert, Christian – sequence: 7 givenname: Tomas surname: Kündig fullname: Kündig, Tomas – sequence: 8 givenname: Michael J. surname: Page fullname: Page, Michael J. – sequence: 9 givenname: Victoria L. surname: Webb fullname: Webb, Victoria L. – sequence: 10 givenname: Jörn surname: Kalinowski fullname: Kalinowski, Jörn – sequence: 11 givenname: Shinichi surname: Sunagawa fullname: Sunagawa, Shinichi – sequence: 12 givenname: Jörn surname: Piel fullname: Piel, Jörn |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32291345$$D View this record in MEDLINE/PubMed |
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| Keywords | microbiomes natural products sponges symbiosis biosynthesis |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by Nancy A. Moran, The University of Texas at Austin, Austin, TX, and approved February 25, 2020 (received for review November 3, 2019) 1M.F.F. and P.N. contributed equally to this work. Author contributions: M.R., E.J.N.H., M.F.F., P.N., C.M.F., C.R., S.S., and J.P. designed research; M.R., E.J.N.H., M.F.F., P.N., C.M.F., C.R., and T.K. performed research; M.J.P. and V.L.W. contributed new reagents/analytic tools; M.J.P. and V.L.W. contributed samples/analyses; M.R., E.J.N.H., M.F.F., P.N., C.M.F., C.R., T.K., M.J.P., V.L.W., J.K., S.S., and J.P. analyzed data; and M.R., E.J.N.H., M.F.F., P.N., C.M.F., C.R., J.K., S.S., and J.P. wrote the paper. |
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| Snippet | Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with... Bacterial specialized metabolites are increasingly recognized as important factors in animal-microbiome interactions: for example, by providing the host with... Sponges, one of the oldest extant animal phyla, stand out among marine organisms as sources of structurally diverse bioactive natural products. Previous work... |
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| SubjectTerms | Bacteria Bioactive compounds Biological Sciences Chemical defense Dark matter Drug development Metabolites Microbiomes Microorganisms Mycale hentscheli Phylogeny Physical Sciences Poisons Symbionts Symbiosis |
| Title | A multiproducer microbiome generates chemical diversity in the marine sponge Mycale hentscheli |
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