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Microbiota Associated with Mollitrichosiphum Aphids (Hemiptera: Aphididae: Greenideinae): Diversity, Host Species Specificity and Phylosymbiosis

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Microbiota Associated with Mollitrichosiphum Aphids (Hemiptera: Aphididae: Greenideinae): Diversity, Host Species Specificity and Phylosymbiosis Environmental Microbiology (2021) 23(4), 2184–2198 doi:10.1111/1462-2920.15391 Microbiota associated with Mollitrichosiphum aphids (Hemiptera: Aphididae: Greenideinae): diversity, host species specificity and phylosymbiosis Man Qin,1,2† Jing Chen ,1† Shifen Xu,1,2 Liyun Jiang1 Introduction and Gexia Qiao 1,2* Eukaryotes engage in associations with a variety of micro- 1Key Laboratory of Zoological Systematics and organisms. Bacterial symbionts of sap-feeding insects Evolution, Institute of Zoology, Chinese Academy of have been documented in numerous studies Sciences, Beijing, China. (Buchner, 1965; Baumann, 2005; Sudakaran et al., 2017). 2College of Life Science, University of Chinese Academy Phloem-feeding aphids and their bacterial symbionts rep- of Sciences, Beijing, China. resent a good model system to study host-symbiont inter- actions. Aphids rely on the primary endosymbiont Summary Buchnera aphidicola, which is located in specialized bac- teriocytes, to supply essential nutrition lacking in their diet Symbiotic association is universal in nature, and an array (Buchner, 1965; Douglas, 1998). Buchnera persists in of symbionts play a crucial part in host life history. almost all aphid species (Baumann et al., 1995), is Aphids and their diverse symbionts have become a good maintained within aphid populations by direct maternal model system to study insect-symbiont interactions. transmission (Koga et al., 2012) and has diversified in par- Previous symbiotic diversity surveys have mainly allel with host lineages (Munson et al., 1991; Clark focused on a few aphid clades, and the relative impor- et al., 2000; Liu et al., 2013; Xu et al., 2018). Furthermore, tance of different factors regulating microbial community Buchnera has undergone extreme gene loss and degrada- structure is not well understood. In this study, we col- tion of functions due to long-term living restricted to bacte- lected 65 colonies representing eight species of the riocytes (Rispe and Moran, 2000; Wernegreen, 2002). In aphid genus Mollitrichosiphum from different regions some aphid species, other bacterial partners are involved and plants in southern China and Nepal and character- in co-obligate associations to compensate for the essential ized their microbial compositions using Illumina nutrient biosynthesis not ensured by Buchnera (e.g., the sequencing of the V3 − V4 hypervariable region of the co-obligate symbiont Serratia symbiotica in Cinara cedri) 16S rRNA gene. We evaluated how microbiota varied (Lamelas et al., 2011; Mccutcheon and Moran, 2012; Ben- across aphid species, geography and host plants and nett and Moran, 2015). the correlation between microbial community structure In addition to the obligate heritable Buchnera, aphids and host aphid phylogeny. Heritable symbionts domi- harbour multiple heritable facultative symbionts that can nated the microbiota associated with Mollitrichosiphum, provide diverse ecological benefits, such as conferring and multiple infections of secondary symbionts were parasitoid and fungal resistance (Oliver et al., 2005; Scar- prevalent. Ordination analyses and statistical tests borough et al., 2005; Łukasik et al., 2013; Heyworth and highlighted the contribution of aphid species in shaping the structures of bacterial, symbiont and secondary sym- Ferrari, 2015), increasing tolerance to heat shock (Chen biont communities. Moreover, we observed a significant et al., 2000; Russell and Moran, 2006; Guay et al., 2009) correlation between Mollitrichosiphum aphid phylogeny and broadening host plant range (Tsuchida et al., 2004; and microbial community composition, providing evi- Tsuchida et al., 2011; Wagner et al., 2015). Facultative dence for a pattern of phylosymbiosis between natural symbionts inhabit various tissues of their aphid hosts aphid populations and their microbial associates. (Oliver et al., 2010) and spread via vertical transmission and occasional horizontal transmission (Russell et al., 2003; Russell and Moran, 2005; Michalik et al., 2014; Pons et al., 2019). Nine facultative symbionts in aphids have Received 19 September, 2020; revised 11 November, 2020; been extensively reported, including Serratia symbiotica accepted 4 January, 2021. *For correspondence. E-mail [email protected]; Tel. +86-10-64807133; Fax +86-10-64807099. (Unterman et al., 1989), Rickettsia (Chen et al., 1996), †These authors contributed equally to this work. Hamiltonella defensa (Darby et al., 2001), Regiella © 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Microbiota of Mollitrichosiphum aphids 2185 insecticola (Sandström et al., 2001), Spiroplasma (Fukatsu communities of eight Mollitrichosiphum species et al., 2001), Arsenophonus (Russell et al., 2003), Fukatsuia collected from different plants and regions across symbiotica (Guay et al., 2009), Rickettsiella viridis southern China and Nepal. We fully assessed the vari- (Tsuchida et al., 2010) and Wolbachia (Augustinos ation in bacterial, symbiont (incl. Buchnera and second- et al., 2011). In aphids, multiple infections of secondary ary symbionts) and secondary symbiont communities symbionts (i.e., infections of more than one symbiont in a according to different factors, including aphid species, host individual) occur moderately because of the cost of geography and host plant, and revealed the microbial harbouring diverse assemblages of secondary symbionts community determinant in Mollitrichosiphum aphids. (Oliver et al., 2014). For example, coinfection of H. defensa Finally, we estimated the correlation between microbial and R. viridis in the pea aphid Acyrthosiphon pisum caused community dissimilarity and aphid relatedness to further a reduction in aphid survival and fecundity (Leclair understand the eco-evolutionary pattern of aphid- et al., 2017). symbiont interactions. To date, most studies on aphid symbiont diversity have focused on the pea aphid and species of subfamilies Aphidinae and Lachninae (Zytynska and Weisser, 2016). Results The occurrence of particular secondary symbionts within Taxonomic composition of the microbial community one aphid species has been reported to be mainly related associated with Mollitrichosiphum aphids to the host plant (Simon et al., 2003; Ferrari et al., 2012; Brady and White, 2013; Gauthier et al., 2015; Xu After all filtering steps, a total of 3,367,211 reads (51,803 et al., 2020a) and geographic distribution (Tsuchida reads per sample) were obtained. Ninety-nine operational et al., 2002). Infection patterns can also vary from native taxonomic units (OTUs) were clustered and assigned to to invasive regions (Bansal et al., 2014) and during sea- 33 genera, 22 families, 15 orders, 13 classes and 6 phyla sonal shifts (Smith et al., 2015; Liu et al., 2019). At taxo- of bacteria. Bacterial communities of Mollitrichosiphum nomic levels higher than species, the patterns of aphids were dominated by the phylum Proteobacteria secondary symbiont infections have been found to be (average relative abundance across all samples: associated with aphid species, characteristics of aphids 99.73%). The most highly dominant class and order were and ecological conditions (Henry et al., 2015; Xu Gammaproteobacteria (93.58%) and Enterobacteriales et al., 2020b, 2021). However, the factors influencing the (93.48%), respectively. Enterobacteriaceae (92.81%) symbiont community structure of aphids have rarely been was the most abundant family, followed by explored and assessed across both ecological and aphid Rickettsiaceae (4.10%) (Table S1). phylogenetic contexts. In addition, more studies on differ- At the genus level, the primary endosymbiont ent aphid lineages are needed for a comprehensive Buchnera was detected in all samples and pre- understanding of the symbiont diversity landscape. dominated in most, with an average relative abun- Mollitrichosiphum is a monophyletic aphid genus of the dance of 72.09%. Six secondary symbionts were subfamily Greenideinae (Insecta: Hemiptera: Aphididae) detected: four showed relative abundances greater that comprises 18 extant species worldwide (11 species than 1% (Serratia symbiotica: 8.91%; Rickettsia: recorded in China) (Favret, 2020) and is mainly distrib- 4.10%; Arsenophonus: 3.10%; Wolbachia: 1.94%), with uted in eastern and southern Asia (Blackman and two having abundances lower than 1% (Fukatsuia Eastop, 2020). Mollitrichosiphum species are monoe- symbiotica: 0.67%; Hamiltonella defensa: 0.40%) (- cious with a holocyclic or anholocyclic life cycle. Some Table S1). S. symbiotica was the most abundant sec- species are monophagous or oligophagous, feeding on ondary symbiont, and its relative abundance was even young leaves or shoots of Fagaceae or Meliosma higher than that of Buchnera in several samples of M. (Sabiaceae); some species colonize plants from different nigrofasciatum (Fig. 1). Additionally, a high frequency families, including Fagaceae, Betulaceae, Sabiaceae, of multiple infections of secondary symbionts was Proteaceae and so on (Ghosh and Agarwala, 1993; observed in Mollitrichosiphum. Each aphid sample Zhang and Qiao, 2010; Blackman and Eastop, 2020). simultaneously harboured 4–6 secondary symbionts. Previous research has confirmed parallel evolution All samples were infected
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