Wang Yin, Rozen Daniel E
Institute of Biology, Leiden University, Leiden, The Netherlands.
Institute of Biology, Leiden University, Leiden, The Netherlands
Appl Environ Microbiol. 2017 Apr 17;83(9). doi: 10.1128/AEM.03250-16. Print 2017 May 1.
Carrion beetles in the genus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization. Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.
属的埋葬虫在腐烂的尸体上养育后代，幼虫会接触到各种各样的分解细菌群落。在卵孵化之前（定义为孵化前照料），亲代用抗菌分泌物覆盖尸体，并且在幼虫的整个发育过程中还会给它们喂食反刍的食物以及可能含有的细菌（定义为全程照料）。在这里，我们区分了孵化前和孵化后亲代照料在可培养共生细菌向幼虫的传播和持续存在中的作用。通过三个处理组（全程照料、仅孵化前照料和无照料），我们发现接受全程照料的幼虫主要被母体肠道中的细菌定殖，而未接受照料的幼虫则被来自尸体的细菌定殖。更重要的是，仅接受孵化前照料的幼虫也主要被母体细菌定殖；这一结果表明，亲代对尸体的处理，包括将细菌应用于尸体表面，即使在没有直接幼虫喂食的情况下也足以确保共生体的转移。在发育后期，我们发现了惊人的证据，即蛹会经历一个无共生体阶段，之后在羽化时它们会被与蜕皮幼虫表皮和蛹室壁上发现的细菌相似的细菌重新定殖。我们的结果阐明了孵化前亲代照料对属中共生体传播的重要性，并表明这些细菌在幼虫和蛹的肠道定殖过程中成功地胜过了分解细菌。在这里，我们研究了埋葬虫幼虫可培养肠道微生物群的起源和持续存在。这种昆虫对于这项研究特别有趣，因为幼虫在腐烂的脊椎动物尸体上饲养，在那里它们会接触到高密度的腐肉分解微生物。幼虫还会以尸体保存和直接幼虫喂食的形式接受广泛的亲代照料。我们发现亲代通过反刍直接将它们肠道中的细菌传递给幼虫，并且通过它们对尸体的影响间接传递。此外，我们发现幼虫在化蛹期间会变成无共生体，但显然在成虫羽化前会被蜕落到昆虫表皮上的细菌重新定殖。我们的结果突出了昆虫行为和发育对微生物群组成的多样相互作用。它们进一步表明，竞争相互作用与甲虫免疫的影响一起或独立介导了幼虫的细菌组成，这表明这些昆虫的细菌群落可能与其宿主物种高度共同进化。
