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Gut bacteria of weevils developing on plant roots under extreme desert conditions

BACKGROUND: Many phytophagous insects, whose diet is generally nitrogen-poor, rely on gut bacteria to compensate for nutritional deficits. Accordingly, we hypothesized that insects in desert environments may evolve associations with gut bacteria to adapt to the extremely low nutrient availability. F...

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Autores principales: Meng, Fengqun, Bar-Shmuel, Nitsan, Shavit, Reut, Behar, Adi, Segoli, Michal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6937996/
https://www.ncbi.nlm.nih.gov/pubmed/31888482
http://dx.doi.org/10.1186/s12866-019-1690-5
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author Meng, Fengqun
Bar-Shmuel, Nitsan
Shavit, Reut
Behar, Adi
Segoli, Michal
author_facet Meng, Fengqun
Bar-Shmuel, Nitsan
Shavit, Reut
Behar, Adi
Segoli, Michal
author_sort Meng, Fengqun
collection PubMed
description BACKGROUND: Many phytophagous insects, whose diet is generally nitrogen-poor, rely on gut bacteria to compensate for nutritional deficits. Accordingly, we hypothesized that insects in desert environments may evolve associations with gut bacteria to adapt to the extremely low nutrient availability. For this, we conducted a systematic survey of bacterial communities in the guts of weevils developing inside mud chambers affixed to plant roots in the Negev Desert of Israel, based on 16S rRNA gene amplicon sequencing. RESULTS: Our analyses revealed that gut bacterial communities in weevil larvae were similar across a wide geographical range, but differed significantly from those of the mud chambers and of the surrounding soils. Nevertheless, a high proportion of bacteria (including all of the core bacteria) found in the weevils were also detected in the mud chambers and soils at low relative abundances. The genus Citrobacter (of the Enterobacteriaceae family) was the predominant group in the guts of all individual weevils. The relative abundance of Citrobacter significantly decreased at the pupal and adult stages, while bacterial diversity increased. A mini literature survey revealed that members of the genus Citrobacter are associated with nitrogen fixation, recycling of uric acid nitrogen, and cellulose degradation in different insects. CONCLUSIONS: The results suggest that although weevils could potentially acquire their gut bacteria from the soil, weevil host internal factors, rather than external environmental factors, were more important in shaping their gut bacterial communities, and suggest a major role for Citrobacter in weevil nutrition in this challenging environment. This study highlights the potential involvement of gut bacteria in the adaptation of insects to nutritional deficiencies under extreme desert conditions.
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spelling pubmed-69379962019-12-31 Gut bacteria of weevils developing on plant roots under extreme desert conditions Meng, Fengqun Bar-Shmuel, Nitsan Shavit, Reut Behar, Adi Segoli, Michal BMC Microbiol Research Article BACKGROUND: Many phytophagous insects, whose diet is generally nitrogen-poor, rely on gut bacteria to compensate for nutritional deficits. Accordingly, we hypothesized that insects in desert environments may evolve associations with gut bacteria to adapt to the extremely low nutrient availability. For this, we conducted a systematic survey of bacterial communities in the guts of weevils developing inside mud chambers affixed to plant roots in the Negev Desert of Israel, based on 16S rRNA gene amplicon sequencing. RESULTS: Our analyses revealed that gut bacterial communities in weevil larvae were similar across a wide geographical range, but differed significantly from those of the mud chambers and of the surrounding soils. Nevertheless, a high proportion of bacteria (including all of the core bacteria) found in the weevils were also detected in the mud chambers and soils at low relative abundances. The genus Citrobacter (of the Enterobacteriaceae family) was the predominant group in the guts of all individual weevils. The relative abundance of Citrobacter significantly decreased at the pupal and adult stages, while bacterial diversity increased. A mini literature survey revealed that members of the genus Citrobacter are associated with nitrogen fixation, recycling of uric acid nitrogen, and cellulose degradation in different insects. CONCLUSIONS: The results suggest that although weevils could potentially acquire their gut bacteria from the soil, weevil host internal factors, rather than external environmental factors, were more important in shaping their gut bacterial communities, and suggest a major role for Citrobacter in weevil nutrition in this challenging environment. This study highlights the potential involvement of gut bacteria in the adaptation of insects to nutritional deficiencies under extreme desert conditions. BioMed Central 2019-12-30 /pmc/articles/PMC6937996/ /pubmed/31888482 http://dx.doi.org/10.1186/s12866-019-1690-5 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Meng, Fengqun
Bar-Shmuel, Nitsan
Shavit, Reut
Behar, Adi
Segoli, Michal
Gut bacteria of weevils developing on plant roots under extreme desert conditions
title Gut bacteria of weevils developing on plant roots under extreme desert conditions
title_full Gut bacteria of weevils developing on plant roots under extreme desert conditions
title_fullStr Gut bacteria of weevils developing on plant roots under extreme desert conditions
title_full_unstemmed Gut bacteria of weevils developing on plant roots under extreme desert conditions
title_short Gut bacteria of weevils developing on plant roots under extreme desert conditions
title_sort gut bacteria of weevils developing on plant roots under extreme desert conditions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6937996/
https://www.ncbi.nlm.nih.gov/pubmed/31888482
http://dx.doi.org/10.1186/s12866-019-1690-5
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