Kanyile Sthandiwe Nomthandazo, Engl Tobias, Heddi Abdelaziz, Kaltenpoth Martin
Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.
INSA Lyon, Université de Lyon, Villeurbanne, France.
Front Microbiol. 2023 Jul 11;14:1199370. doi: 10.3389/fmicb.2023.1199370. eCollection 2023.
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, 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 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.
昆虫常常与细胞内微生物共生体（内共生体）相关联，这些共生体可增强它们应对具有挑战性的环境条件的能力。在几个甲虫科中都报道过与增强角质层的微生物形成的内共生关系。然而，这些关联的生态相关性很少得到证实，特别是在干燥环境中，高质量的角质层可以减少水分流失的情况下。因此，我们研究了米象的角质层增强共生体如何有助于提高抗干燥能力。我们将有共生体和无共生体（aposymbiotic，即无菌）的甲虫暴露于长期的应激（47%相对湿度）或宽松（60%相对湿度）湿度条件下，并测量种群增长情况。我们发现，共生体的存在有利于宿主的适应性，尤其是在干燥条件下，使有共生体的甲虫能够在3个月内将种群数量增加超过33倍，而在相同条件下，无菌甲虫的数量未能超过初始种群数量。为了了解这种显著效果背后的机制，我们比较了甲虫的大小和体内含水量，发现内共生体赋予了更大的体型和更高的体内含水量。虽然化学分析显示，在长期暴露于干燥胁迫后，表皮碳氢化合物的组成和数量没有显著差异，但有共生体的甲虫失水速度比无菌甲虫慢。我们认为，在干燥条件下有共生体的甲虫表现出的抗干燥能力和更高的适应性是由于它们的共生体增强了角质层厚度，从而提供了防止角质层蒸腾的保护。因此，我们证明了米象的角质层增强共生关系在干旱胁迫下赋予了适应性优势，干旱胁迫是谷物害虫甲虫的一个生态相关条件。这种优势可能扩展到许多其他已鉴定出共生体介导角质层合成的系统，包括跨越占据不同生态位的甲虫和蚂蚁的分类群。
