Tissue- and Population-Level Microbiome Analysis of the Wasp Spider Argiope bruennichi Identified a Novel Dominant Bacterial Symbiont

Abstract

Many ecological and evolutionary processes in animals depend upon microbial symbioses. In spiders, the role of the microbiome in these processes remains mostly unknown. We compared the microbiome between populations, individuals, and tissue types of a range-expanding spider, using 16S rRNA gene sequencing. Our study is one of the first to go beyond targeting known endosymbionts in spiders and characterizes the total microbiome across different body compartments (leg, prosoma, hemolymph, book lungs, ovaries, silk glands, midgut, and fecal pellets). Overall, the microbiome differed significantly between populations and individuals, but not between tissue types. The microbiome of the wasp spider Argiope bruennichi features a novel dominant bacterial symbiont, which is abundant in every tissue type in spiders from geographically distinct populations and that is also present in offspring. The novel symbiont is affiliated with the Tenericutes, but has low sequence identity (<85%) to all previously named taxa, suggesting that the novel symbiont represents a new bacterial clade. Its presence in offspring implies that it is vertically transmitted. Our results shed light on the processes that shape microbiome differentiation in this species and raise several questions about the implications of the novel dominant bacterial symbiont on the biology and evolution of its host.

Microbiomes and Specific Symbionts of Social Spiders: Compositional Patterns in Host Species, Populations, and Nests

“…The simple microbiome structure observed in the individuals of all three social Stegodyphus species, with low alpha diversity, strong dominance of 1-2 bacterial species (or ASVs), and a core microbiome of <10 species (Figures 2, 3, and Supplementary Figure S1), appears typical for the gut microbiomes of social arthropods (Corby-Harris et al, 2014;Sapountzis et al, 2015), with the notable exception of wood-feeding termites that rely on a complex microbiome for lignocellulose degradation (Benjamino and Graf, 2016). Solitary spider microbiomes are generally of low diversity (Zhang et al, 2018), and tend to be even more dominated by single symbionts than the social arthropods (Sheffer et al, 2020;White et al, 2020). With the current study design, we cannot deduce if the observed microbiome structure is specific for social Stegodyphus species or more general for the genus Stegodyphus.…”

Chromosome-level reference genome of the European wasp spiderArgiope bruennichi: a resource for studies on range expansion and evolutionary adaptation

“…BlobTools (v. 1.0) (Blobtools, RRID:SCR_017618) [46] was used to search for contamination, and subsequently mitochondrial sequences and bacterial scaffolds were removed from the assembly. The 14 th -largest scaffold (Scaffold 839) matched the sequence of a recently-discovered bacterial symbiont of Argiope bruennichi [47].…”

Does sexual cannibalism secure genetic benefits of polyandry in a size-dimorphic spider?

“…For example, in the dwarf spider Oedothorax gibbosus, clutches of Wolbachia-infected females are significantly female biased (Vanthournout et al 2011), and infection with Rickettsia bacteria lowers the tendency for long-distance dispersal behavior ("ballooning") in another dwarf spider, Erigone atra (Goodacre et al 2009). In A. bruennichi, no known endosymbionts have been found so far (Duron et al 2008;Yun et al 2011;Sheffer et al 2020). Yet, a recent microbiome analysis detected a novel dominant bacterium that is related to the Mollicutes (Sheffer et al 2020), a bacterial class containing many arthropod-associated endosymbionts (e.g., Meeus et al 2012;Sapountzis et al 2018).…”

“…Yet, a recent microbiome analysis detected a novel dominant bacterium that is related to the Mollicutes (Sheffer et al 2020), a bacterial class containing many arthropod-associated endosymbionts (e.g., Meeus et al 2012;Sapountzis et al 2018). Given that this bacterium might actually constitute a novel endosymbiont of A. bruennichi (Sheffer et al 2020), it is tempting to speculate whether it might have any influence on the mating system of A. bruennichi including selection for polyandry.…”