Liaoning Key Laboratory of Economic and Applied Entomology, College of Plant Protection, Shenyang Agricultural University, Shenyang, 110866, China.
Department of Botany and Plant Sciences, Center for Plant Cell Biology, University of California, Riverside, CA, 92521-0124, USA.
ISME J. 2020 Dec;14(12):2923-2935. doi: 10.1038/s41396-020-0717-0. Epub 2020 Jul 20.
Symbionts can regulate animal reproduction in multiple ways, but the underlying physiological and biochemical mechanisms remain largely unknown. The presence of multiple lineages of maternally inherited, intracellular symbionts (the primary and secondary symbionts) in terrestrial arthropods is widespread in nature. However, the biological, metabolic, and evolutionary role of co-resident secondary symbionts for hosts is poorly understood. The bacterial symbionts Hamiltonella and Arsenophonus have very high prevalence in two globally important pests, the whiteflies Bemisia tabaci and Trialeurodes vaporariorum, respectively. Both symbionts coexist with the primary symbiont Portiera in the same host cell (bacteriocyte) and are maternally transmitted. We found that elimination of both Hamiltonella and Arsenophonous by antibiotic treatment reduced the percentage of female offspring in whiteflies. Microsatellite genotyping and cytogenetic analysis revealed that symbiont deficiency inhibited fertilization in whiteflies, leading to more haploid males with one maternal allele, which is consistent with distorted sex ratio in whiteflies. Quantification of essential amino acids and B vitamins in whiteflies indicated that symbiont deficiency reduced B vitamin levels, and dietary B vitamin supplementation rescued fitness of whiteflies. This study, for the first time, conclusively demonstrates that these two intracellular symbionts affect sex ratios in their whitefly hosts by regulating fertilization and supplying B vitamins. Our results reveal that both symbionts have the convergent function of regulating reproduction in phylogenetically-distant whitefly species. The 100% frequency, the inability of whiteflies to develop normally without their symbiont, and rescue with B vitamins suggests that both symbionts may be better considered co-primary symbionts.
共生体可以通过多种方式调节动物的繁殖，但其中的生理和生化机制在很大程度上仍然未知。在陆生节肢动物中，存在多种母系遗传的内共生体（初级和次级共生体），这在自然界中非常普遍。然而，共生的次级共生体对宿主的生物学、代谢和进化作用还知之甚少。细菌共生体 Hamiltonella 和 Arsenophonus 分别在两种全球重要的害虫——烟粉虱和温室粉虱中广泛存在。这两种共生体与初级共生体 Portiera 共存于同一宿主细胞（质体）中，并通过母系遗传传递。我们发现，抗生素处理消除 Hamiltonella 和 Arsenophonus 会降低粉虱中雌性后代的比例。微卫星基因分型和细胞遗传学分析表明，共生体缺陷抑制了粉虱的受精，导致更多的单倍体雄性，只有一个母体等位基因，这与粉虱中性别比例的扭曲一致。对粉虱中必需氨基酸和 B 族维生素的定量分析表明，共生体缺陷降低了 B 族维生素水平，而膳食 B 族维生素补充则挽救了粉虱的适应性。这项研究首次明确证明，这两种内共生体通过调节受精和提供 B 族维生素来影响其粉虱宿主的性别比例。我们的结果表明，这两种共生体具有调节亲缘关系较远的粉虱物种生殖的趋同功能。100%的频率、粉虱没有共生体就无法正常发育以及 B 族维生素的拯救作用表明，这两种共生体可能更好地被认为是共同的初级共生体。
