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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...

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Autores principales: Kanyile, Sthandiwe Nomthandazo, Engl, Tobias, Heddi, Abdelaziz, Kaltenpoth, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
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.
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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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