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Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome

Larval net-spinning caddisflies (Hydropsychidae) function as ecosystem engineers in streams where they construct protective retreats composed of organic and inorganic material affixed with silk filtration nets that alter streambed hydrology. We hypothesized that hydropsychid bio-structures (retreats...

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Autores principales: Bertagnolli, Anthony D., Maritan, Andrew J., Tumolo, Benjamin B., Fritz, Samuel F., Oakland, Hayley C., Mohr, Elizabeth J., Poole, Geoffrey C., Albertson, Lindsey K., Stewart, Frank J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10582121/
https://www.ncbi.nlm.nih.gov/pubmed/37848489
http://dx.doi.org/10.1038/s43705-023-00315-8
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author Bertagnolli, Anthony D.
Maritan, Andrew J.
Tumolo, Benjamin B.
Fritz, Samuel F.
Oakland, Hayley C.
Mohr, Elizabeth J.
Poole, Geoffrey C.
Albertson, Lindsey K.
Stewart, Frank J.
author_facet Bertagnolli, Anthony D.
Maritan, Andrew J.
Tumolo, Benjamin B.
Fritz, Samuel F.
Oakland, Hayley C.
Mohr, Elizabeth J.
Poole, Geoffrey C.
Albertson, Lindsey K.
Stewart, Frank J.
author_sort Bertagnolli, Anthony D.
collection PubMed
description Larval net-spinning caddisflies (Hydropsychidae) function as ecosystem engineers in streams where they construct protective retreats composed of organic and inorganic material affixed with silk filtration nets that alter streambed hydrology. We hypothesized that hydropsychid bio-structures (retreats, nets) are microhabitats for microbes with oxygen-sensitive metabolisms, and therefore increase the metabolic heterogeneity of streambed microbial assemblages. Metagenomic and 16 S rRNA gene amplicon analysis of samples from a montane stream (Cherry Creek, Montana, USA) revealed that microbiomes of caddisfly bio-structures are taxonomically and functionally distinct from those of the immediately adjacent rock biofilm (~2 cm distant) and enriched in microbial taxa with established roles in denitrification, nitrification, and methane production. Genes for denitrification, high oxygen affinity terminal oxidases, hydrogenases, oxidative dissimilatory sulfite reductases, and complete ammonia oxidation are significantly enriched in caddisfly bio-structures. The results suggest a novel ecosystem engineering effect of caddisflies through the creation of low-oxygen, denitrifier-enriched niches in the stream microbiome. Facilitation of metabolic diversity in streambeds may be a largely unrecognized mechanism by which caddisflies alter whole-stream biogeochemistry.
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spelling pubmed-105821212023-10-19 Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome Bertagnolli, Anthony D. Maritan, Andrew J. Tumolo, Benjamin B. Fritz, Samuel F. Oakland, Hayley C. Mohr, Elizabeth J. Poole, Geoffrey C. Albertson, Lindsey K. Stewart, Frank J. ISME Commun Brief Communication Larval net-spinning caddisflies (Hydropsychidae) function as ecosystem engineers in streams where they construct protective retreats composed of organic and inorganic material affixed with silk filtration nets that alter streambed hydrology. We hypothesized that hydropsychid bio-structures (retreats, nets) are microhabitats for microbes with oxygen-sensitive metabolisms, and therefore increase the metabolic heterogeneity of streambed microbial assemblages. Metagenomic and 16 S rRNA gene amplicon analysis of samples from a montane stream (Cherry Creek, Montana, USA) revealed that microbiomes of caddisfly bio-structures are taxonomically and functionally distinct from those of the immediately adjacent rock biofilm (~2 cm distant) and enriched in microbial taxa with established roles in denitrification, nitrification, and methane production. Genes for denitrification, high oxygen affinity terminal oxidases, hydrogenases, oxidative dissimilatory sulfite reductases, and complete ammonia oxidation are significantly enriched in caddisfly bio-structures. The results suggest a novel ecosystem engineering effect of caddisflies through the creation of low-oxygen, denitrifier-enriched niches in the stream microbiome. Facilitation of metabolic diversity in streambeds may be a largely unrecognized mechanism by which caddisflies alter whole-stream biogeochemistry. Nature Publishing Group UK 2023-10-17 /pmc/articles/PMC10582121/ /pubmed/37848489 http://dx.doi.org/10.1038/s43705-023-00315-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Brief Communication
Bertagnolli, Anthony D.
Maritan, Andrew J.
Tumolo, Benjamin B.
Fritz, Samuel F.
Oakland, Hayley C.
Mohr, Elizabeth J.
Poole, Geoffrey C.
Albertson, Lindsey K.
Stewart, Frank J.
Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
title Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
title_full Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
title_fullStr Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
title_full_unstemmed Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
title_short Net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
title_sort net-spinning caddisflies create denitrifier-enriched niches in the stream microbiome
topic Brief Communication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10582121/
https://www.ncbi.nlm.nih.gov/pubmed/37848489
http://dx.doi.org/10.1038/s43705-023-00315-8
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