Gut microbiomes of cycad-feeding insects tolerant to β-methylamino-L-alanine (BMAA) are rich in siderophore biosynthesis.


Journal

ISME communications
ISSN: 2730-6151
Titre abrégé: ISME Commun
Pays: England
ID NLM: 9918205372406676

Informations de publication

Date de publication:
22 Nov 2023
Historique:
received: 02 05 2023
accepted: 25 10 2023
revised: 17 10 2023
medline: 23 11 2023
pubmed: 23 11 2023
entrez: 22 11 2023
Statut: epublish

Résumé

Ingestion of the cycad toxins β-methylamino-L-alanine (BMAA) and azoxyglycosides is harmful to diverse organisms. However, some insects are specialized to feed on toxin-rich cycads with apparent immunity. Some cycad-feeding insects possess a common set of gut bacteria, which might play a role in detoxifying cycad toxins. Here, we investigated the composition of gut microbiota from a worldwide sample of cycadivorous insects and characterized the biosynthetic potential of selected bacteria. Cycadivorous insects shared a core gut microbiome consisting of six bacterial taxa, mainly belonging to the Proteobacteria, which we were able to isolate. To further investigate selected taxa from diverging lineages, we performed shotgun metagenomic sequencing of co-cultured bacterial sub-communities. We characterized the biosynthetic potential of four bacteria from Serratia, Pantoea, and two different Stenotrophomonas lineages, and discovered a suite of biosynthetic gene clusters notably rich in siderophores. Siderophore semi-untargeted metabolomics revealed a broad range of chemically related yet diverse iron-chelating metabolites, including desferrioxamine B, suggesting the occurrence of an unprecedented desferrioxamine-like biosynthetic pathway that remains to be identified. These results provide a foundation for future investigations into how cycadivorous insects tolerate diets rich in azoxyglycosides, BMAA, and other cycad toxins, including a possible role for bacterial siderophores.

Identifiants

pubmed: 37993724
doi: 10.1038/s43705-023-00323-8
pii: 10.1038/s43705-023-00323-8
pmc: PMC10665472
doi:

Types de publication

Journal Article

Langues

eng

Pagination

122

Subventions

Organisme : National Science Foundation (NSF)
ID : 1541560, 1309425, 1906333
Organisme : Newton Fund
ID : NAF/R2/180631
Organisme : Consejo Nacional de Ciencia y Tecnología (National Council of Science and Technology, Mexico)
ID : 169701, 179290, 177568, FON.INST./265/2016 285746,

Informations de copyright

© 2023. The Author(s).

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Auteurs

Karina Gutiérrez-García (K)

Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Km 9.6 Libramiento Irapuato - León, Irapuato, Guanajuato, 36824, México.
Department of Embryology, Carnegie Institution for Science, 3520 San Martin Drive, Baltimore, MD, 21218, USA.

Melissa R L Whitaker (MRL)

Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA. melliwhitaker@gmail.com.
Department of Biological Sciences, East Tennessee State University, Johnson City, TN, 37614, USA. melliwhitaker@gmail.com.

Edder D Bustos-Díaz (ED)

Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Km 9.6 Libramiento Irapuato - León, Irapuato, Guanajuato, 36824, México.
Institute of Biology, Leiden University, Sylviusweg 72, Leiden, 2333 BE, The Netherlands.

Shayla Salzman (S)

Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.
University of Georgia, Entomology Department, Athens, GA, 30602, USA.

Hilda E Ramos-Aboites (HE)

Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Km 9.6 Libramiento Irapuato - León, Irapuato, Guanajuato, 36824, México.

Zachary L Reitz (ZL)

Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708PB, Wageningen, The Netherlands.

Naomi E Pierce (NE)

Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.

Angélica Cibrián-Jaramillo (A)

Ecological and Evolutionary Genomics Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Km 9.6 Libramiento Irapuato - León, Irapuato, Guanajuato, 36824, México.
Naturalis Biodiversity Center, Darwinweg 2, 2333 CR, Leiden, The Netherlands.

Francisco Barona-Gómez (F)

Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Km 9.6 Libramiento Irapuato - León, Irapuato, Guanajuato, 36824, México. f.barona.gomez@biology.leidenuniv.nl.
Institute of Biology, Leiden University, Sylviusweg 72, Leiden, 2333 BE, The Netherlands. f.barona.gomez@biology.leidenuniv.nl.

Classifications MeSH