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Endosymbiosis allows Sitophilus oryzae to persist in dry conditions
Insects frequently associate with intracellular microbial symbionts (endosymbionts) that enhance their ability to cope with challenging environmental conditions. Endosymbioses with cuticle-enhancing microbes have been reported in several beetle families. However, the ecological relevance of these as...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10366622/ https://www.ncbi.nlm.nih.gov/pubmed/37497544 http://dx.doi.org/10.3389/fmicb.2023.1199370 |
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author | Kanyile, Sthandiwe Nomthandazo Engl, Tobias Heddi, Abdelaziz Kaltenpoth, Martin |
author_facet | Kanyile, Sthandiwe Nomthandazo Engl, Tobias Heddi, Abdelaziz Kaltenpoth, Martin |
author_sort | Kanyile, Sthandiwe Nomthandazo |
collection | PubMed |
description | Insects frequently associate with intracellular microbial symbionts (endosymbionts) that enhance their ability to cope with challenging environmental conditions. Endosymbioses with cuticle-enhancing microbes have been reported in several beetle families. However, the ecological relevance of these associations has seldom been demonstrated, particularly in the context of dry environments where high cuticle quality can reduce water loss. Thus, we investigated how cuticle-enhancing symbionts of the rice-weevil, Sitophilus oryzae contribute to desiccation resistance. We exposed symbiotic and symbiont-free (aposymbiotic) beetles to long-term stressful (47% RH) or relaxed (60% RH) humidity conditions and measured population growth. We found that symbiont presence benefits host fitness especially under dry conditions, enabling symbiotic beetles to increase their population size by over 33-fold within 3 months, while aposymbiotic beetles fail to increase in numbers beyond the starting population in the same conditions. To understand the mechanisms underlying this drastic effect, we compared beetle size and body water content and found that endosymbionts confer bigger body size and higher body water content. While chemical analyses revealed no significant differences in composition and quantity of cuticular hydrocarbons after long-term exposure to desiccation stress, symbiotic beetles lost water at a proportionally slower rate than did their aposymbiotic counterparts. We posit that the desiccation resistance and higher fitness observed in symbiotic beetles under dry conditions is due to their symbiont-enhanced thicker cuticle, which provides protection against cuticular transpiration. Thus, we demonstrate that the cuticle enhancing symbiosis of Sitophilus oryzae confers a fitness benefit under drought stress, an ecologically relevant condition for grain pest beetles. This benefit likely extends to many other systems where symbiont-mediated cuticle synthesis has been identified, including taxa spanning beetles and ants that occupy different ecological niches. |
format | Online Article Text |
id | pubmed-10366622 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-103666222023-07-26 Endosymbiosis allows Sitophilus oryzae to persist in dry conditions Kanyile, Sthandiwe Nomthandazo Engl, Tobias Heddi, Abdelaziz Kaltenpoth, Martin Front Microbiol Microbiology Insects frequently associate with intracellular microbial symbionts (endosymbionts) that enhance their ability to cope with challenging environmental conditions. Endosymbioses with cuticle-enhancing microbes have been reported in several beetle families. However, the ecological relevance of these associations has seldom been demonstrated, particularly in the context of dry environments where high cuticle quality can reduce water loss. Thus, we investigated how cuticle-enhancing symbionts of the rice-weevil, Sitophilus oryzae contribute to desiccation resistance. We exposed symbiotic and symbiont-free (aposymbiotic) beetles to long-term stressful (47% RH) or relaxed (60% RH) humidity conditions and measured population growth. We found that symbiont presence benefits host fitness especially under dry conditions, enabling symbiotic beetles to increase their population size by over 33-fold within 3 months, while aposymbiotic beetles fail to increase in numbers beyond the starting population in the same conditions. To understand the mechanisms underlying this drastic effect, we compared beetle size and body water content and found that endosymbionts confer bigger body size and higher body water content. While chemical analyses revealed no significant differences in composition and quantity of cuticular hydrocarbons after long-term exposure to desiccation stress, symbiotic beetles lost water at a proportionally slower rate than did their aposymbiotic counterparts. We posit that the desiccation resistance and higher fitness observed in symbiotic beetles under dry conditions is due to their symbiont-enhanced thicker cuticle, which provides protection against cuticular transpiration. Thus, we demonstrate that the cuticle enhancing symbiosis of Sitophilus oryzae confers a fitness benefit under drought stress, an ecologically relevant condition for grain pest beetles. This benefit likely extends to many other systems where symbiont-mediated cuticle synthesis has been identified, including taxa spanning beetles and ants that occupy different ecological niches. Frontiers Media S.A. 2023-07-11 /pmc/articles/PMC10366622/ /pubmed/37497544 http://dx.doi.org/10.3389/fmicb.2023.1199370 Text en Copyright © 2023 Kanyile, Engl, Heddi and Kaltenpoth. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Kanyile, Sthandiwe Nomthandazo Engl, Tobias Heddi, Abdelaziz Kaltenpoth, Martin Endosymbiosis allows Sitophilus oryzae to persist in dry conditions |
title | Endosymbiosis allows Sitophilus oryzae to persist in dry conditions |
title_full | Endosymbiosis allows Sitophilus oryzae to persist in dry conditions |
title_fullStr | Endosymbiosis allows Sitophilus oryzae to persist in dry conditions |
title_full_unstemmed | Endosymbiosis allows Sitophilus oryzae to persist in dry conditions |
title_short | Endosymbiosis allows Sitophilus oryzae to persist in dry conditions |
title_sort | endosymbiosis allows sitophilus oryzae to persist in dry conditions |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10366622/ https://www.ncbi.nlm.nih.gov/pubmed/37497544 http://dx.doi.org/10.3389/fmicb.2023.1199370 |
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