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The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei

Teredinidae are a family of highly adapted wood-feeding and wood-boring bivalves, commonly known as shipworms, whose evolution is linked to the acquisition of cellulolytic gammaproteobacterial symbionts harbored in bacteriocytes within the gills. In the present work we applied metagenomics to charac...

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Autores principales: Brito, Thais L., Campos, Amanda B., Bastiaan von Meijenfeldt, F. A., Daniel, Julio P., Ribeiro, Gabriella B., Silva, Genivaldo G. Z., Wilke, Diego V., de Moraes, Daniela T., Dutilh, Bas E., Meirelles, Pedro M., Trindade-Silva, Amaro E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6235255/
https://www.ncbi.nlm.nih.gov/pubmed/30427852
http://dx.doi.org/10.1371/journal.pone.0200437
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author Brito, Thais L.
Campos, Amanda B.
Bastiaan von Meijenfeldt, F. A.
Daniel, Julio P.
Ribeiro, Gabriella B.
Silva, Genivaldo G. Z.
Wilke, Diego V.
de Moraes, Daniela T.
Dutilh, Bas E.
Meirelles, Pedro M.
Trindade-Silva, Amaro E.
author_facet Brito, Thais L.
Campos, Amanda B.
Bastiaan von Meijenfeldt, F. A.
Daniel, Julio P.
Ribeiro, Gabriella B.
Silva, Genivaldo G. Z.
Wilke, Diego V.
de Moraes, Daniela T.
Dutilh, Bas E.
Meirelles, Pedro M.
Trindade-Silva, Amaro E.
author_sort Brito, Thais L.
collection PubMed
description Teredinidae are a family of highly adapted wood-feeding and wood-boring bivalves, commonly known as shipworms, whose evolution is linked to the acquisition of cellulolytic gammaproteobacterial symbionts harbored in bacteriocytes within the gills. In the present work we applied metagenomics to characterize microbiomes of the gills and digestive tract of Neoteredo reynei, a mangrove-adapted shipworm species found over a large range of the Brazilian coast. Comparative metagenomics grouped the gill symbiont community of different N. reynei specimens, indicating closely related bacterial types are shared. Similarly, the intestine and digestive gland communities were related, yet were more diverse than and showed no overlap with the gill community. Annotation of assembled metagenomic contigs revealed that the gill symbiotic community of N. reynei encodes a plethora of plant cell wall polysaccharides degrading glycoside hydrolase encoding genes, and Biosynthetic Gene Clusters (BGCs). In contrast, the digestive tract microbiomes seem to play little role in wood digestion and secondary metabolites biosynthesis. Metagenome binning recovered the nearly complete genome sequences of two symbiotic Teredinibacter strains from the gills, a representative of Teredinibacter turnerae “clade I” strain, and a yet to be cultivated Teredinibacter sp. type. These Teredinibacter genomes, as well as un-binned gill-derived gammaproteobacteria contigs, also include an endo-β-1,4-xylanase/acetylxylan esterase multi-catalytic carbohydrate-active enzyme, and a trans-acyltransferase polyketide synthase (trans-AT PKS) gene cluster with the gene cassette for generating β-branching on complex polyketides. Finally, we use multivariate analyses to show that the secondary metabolome from the genomes of Teredinibacter representatives, including genomes binned from N. reynei gills’ metagenomes presented herein, stands out within the Cellvibrionaceae family by size, and enrichments for polyketide, nonribosomal peptide and hybrid BGCs. Results presented here add to the growing characterization of shipworm symbiotic microbiomes and indicate that the N. reynei gill gammaproteobacterial community is a prolific source of biotechnologically relevant enzymes for wood-digestion and bioactive compounds production.
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spelling pubmed-62352552018-12-01 The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei Brito, Thais L. Campos, Amanda B. Bastiaan von Meijenfeldt, F. A. Daniel, Julio P. Ribeiro, Gabriella B. Silva, Genivaldo G. Z. Wilke, Diego V. de Moraes, Daniela T. Dutilh, Bas E. Meirelles, Pedro M. Trindade-Silva, Amaro E. PLoS One Research Article Teredinidae are a family of highly adapted wood-feeding and wood-boring bivalves, commonly known as shipworms, whose evolution is linked to the acquisition of cellulolytic gammaproteobacterial symbionts harbored in bacteriocytes within the gills. In the present work we applied metagenomics to characterize microbiomes of the gills and digestive tract of Neoteredo reynei, a mangrove-adapted shipworm species found over a large range of the Brazilian coast. Comparative metagenomics grouped the gill symbiont community of different N. reynei specimens, indicating closely related bacterial types are shared. Similarly, the intestine and digestive gland communities were related, yet were more diverse than and showed no overlap with the gill community. Annotation of assembled metagenomic contigs revealed that the gill symbiotic community of N. reynei encodes a plethora of plant cell wall polysaccharides degrading glycoside hydrolase encoding genes, and Biosynthetic Gene Clusters (BGCs). In contrast, the digestive tract microbiomes seem to play little role in wood digestion and secondary metabolites biosynthesis. Metagenome binning recovered the nearly complete genome sequences of two symbiotic Teredinibacter strains from the gills, a representative of Teredinibacter turnerae “clade I” strain, and a yet to be cultivated Teredinibacter sp. type. These Teredinibacter genomes, as well as un-binned gill-derived gammaproteobacteria contigs, also include an endo-β-1,4-xylanase/acetylxylan esterase multi-catalytic carbohydrate-active enzyme, and a trans-acyltransferase polyketide synthase (trans-AT PKS) gene cluster with the gene cassette for generating β-branching on complex polyketides. Finally, we use multivariate analyses to show that the secondary metabolome from the genomes of Teredinibacter representatives, including genomes binned from N. reynei gills’ metagenomes presented herein, stands out within the Cellvibrionaceae family by size, and enrichments for polyketide, nonribosomal peptide and hybrid BGCs. Results presented here add to the growing characterization of shipworm symbiotic microbiomes and indicate that the N. reynei gill gammaproteobacterial community is a prolific source of biotechnologically relevant enzymes for wood-digestion and bioactive compounds production. Public Library of Science 2018-11-14 /pmc/articles/PMC6235255/ /pubmed/30427852 http://dx.doi.org/10.1371/journal.pone.0200437 Text en © 2018 Brito et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Brito, Thais L.
Campos, Amanda B.
Bastiaan von Meijenfeldt, F. A.
Daniel, Julio P.
Ribeiro, Gabriella B.
Silva, Genivaldo G. Z.
Wilke, Diego V.
de Moraes, Daniela T.
Dutilh, Bas E.
Meirelles, Pedro M.
Trindade-Silva, Amaro E.
The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei
title The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei
title_full The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei
title_fullStr The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei
title_full_unstemmed The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei
title_short The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei
title_sort gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm neoteredo reynei
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6235255/
https://www.ncbi.nlm.nih.gov/pubmed/30427852
http://dx.doi.org/10.1371/journal.pone.0200437
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