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Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae)
Gut microbes play an important role in the biology and evolution of insects. Australian native dung beetles (Scarabaeinae) present an opportunity to study gut microbiota in an evolutionary context as they come from two distinct phylogenetic lineages and some species in each lineage have secondarily...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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American Society for Microbiology
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8090880/ https://www.ncbi.nlm.nih.gov/pubmed/33355113 http://dx.doi.org/10.1128/AEM.02100-20 |
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author | Ebert, Kathryn M. Arnold, William G. Ebert, Paul R. Merritt, David J. |
author_facet | Ebert, Kathryn M. Arnold, William G. Ebert, Paul R. Merritt, David J. |
author_sort | Ebert, Kathryn M. |
collection | PubMed |
description | Gut microbes play an important role in the biology and evolution of insects. Australian native dung beetles (Scarabaeinae) present an opportunity to study gut microbiota in an evolutionary context as they come from two distinct phylogenetic lineages and some species in each lineage have secondarily adapted to alternative or broader diets. In this study, we characterized the hindgut bacterial communities found in 21 species of dung beetles across two lineages, using 16S rRNA sequencing. We found that gut microbial diversity was more dependent on host phylogeny and gut morphology than specific dietary preferences or environment. In particular, gut microbial diversity was highest in the endemic, flightless genus Cephalodesmius, which feeds on a broad range of composted organic matter. The hindgut of Cephalodesmius beetles harbors a highly conserved core set of bacteria, suggesting that the bacteria are symbiotic. Symbiosis is supported by the persistence of the core microbiota across isolated beetle populations and between species in the genus. A coevolutionary relationship is supported by the expansion of the hindgut to form a fermentation chamber and the fermentative nature of the core microbes. In contrast, Australian species of the widespread dung beetle genus Onthophagus that specialize on a single food resource, such as dung or fungus, exhibit minimal food processing behavior and have a short, narrow hindgut and a variable gut microbiota with relatively few core bacterial taxa. A conserved, complex gut microbiota is hypothesized to be unnecessary for this highly mobile genus. IMPORTANCE Dung beetles are a very important part of an ecosystem because of their role in the removal and decomposition of vertebrate dung. It has been suspected that symbiotic gut bacteria facilitate this role, a hypothesis that we have explored with high-throughput barcoding. We found that differences in hindgut morphology had the greatest effect on the bacterial community composition. Species with a hindgut fermentation chamber harbored a distinctly different hindgut community compared to those species with a narrow, undifferentiated hindgut. Diet and phylogeny were also associated with differences in gut community. Further understanding of the relationships between dung beetles and their gut microbes will provide insights into the evolution of their behaviors and how gut communities contribute to their fitness. |
format | Online Article Text |
id | pubmed-8090880 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-80908802021-08-12 Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) Ebert, Kathryn M. Arnold, William G. Ebert, Paul R. Merritt, David J. Appl Environ Microbiol Invertebrate Microbiology Gut microbes play an important role in the biology and evolution of insects. Australian native dung beetles (Scarabaeinae) present an opportunity to study gut microbiota in an evolutionary context as they come from two distinct phylogenetic lineages and some species in each lineage have secondarily adapted to alternative or broader diets. In this study, we characterized the hindgut bacterial communities found in 21 species of dung beetles across two lineages, using 16S rRNA sequencing. We found that gut microbial diversity was more dependent on host phylogeny and gut morphology than specific dietary preferences or environment. In particular, gut microbial diversity was highest in the endemic, flightless genus Cephalodesmius, which feeds on a broad range of composted organic matter. The hindgut of Cephalodesmius beetles harbors a highly conserved core set of bacteria, suggesting that the bacteria are symbiotic. Symbiosis is supported by the persistence of the core microbiota across isolated beetle populations and between species in the genus. A coevolutionary relationship is supported by the expansion of the hindgut to form a fermentation chamber and the fermentative nature of the core microbes. In contrast, Australian species of the widespread dung beetle genus Onthophagus that specialize on a single food resource, such as dung or fungus, exhibit minimal food processing behavior and have a short, narrow hindgut and a variable gut microbiota with relatively few core bacterial taxa. A conserved, complex gut microbiota is hypothesized to be unnecessary for this highly mobile genus. IMPORTANCE Dung beetles are a very important part of an ecosystem because of their role in the removal and decomposition of vertebrate dung. It has been suspected that symbiotic gut bacteria facilitate this role, a hypothesis that we have explored with high-throughput barcoding. We found that differences in hindgut morphology had the greatest effect on the bacterial community composition. Species with a hindgut fermentation chamber harbored a distinctly different hindgut community compared to those species with a narrow, undifferentiated hindgut. Diet and phylogeny were also associated with differences in gut community. Further understanding of the relationships between dung beetles and their gut microbes will provide insights into the evolution of their behaviors and how gut communities contribute to their fitness. American Society for Microbiology 2021-02-12 /pmc/articles/PMC8090880/ /pubmed/33355113 http://dx.doi.org/10.1128/AEM.02100-20 Text en Copyright © 2021 Ebert et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Invertebrate Microbiology Ebert, Kathryn M. Arnold, William G. Ebert, Paul R. Merritt, David J. Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) |
title | Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) |
title_full | Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) |
title_fullStr | Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) |
title_full_unstemmed | Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) |
title_short | Hindgut Microbiota Reflects Different Digestive Strategies in Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae) |
title_sort | hindgut microbiota reflects different digestive strategies in dung beetles (coleoptera: scarabaeidae: scarabaeinae) |
topic | Invertebrate Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8090880/ https://www.ncbi.nlm.nih.gov/pubmed/33355113 http://dx.doi.org/10.1128/AEM.02100-20 |
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