Temporal and spatial microbiome dynamics across natural populations of the social spider Stegodyphus dumicola

Abstract

Host symbiont interactions may form obligatory or facultative associations that are context dependent. Long-term studies on microbiome composition from wild populations should assess the temporal and spatial dynamics of host-microbe associations. We characterized the temporal and spatial variation in the bacterial microbiome composition in six populations of the social spider Stegodyphus dumicola for 2.5 years, using 16S rRNA gene amplicon sequencing of whole spiders. Individuals within a nest exhibit highly similar microbiomes, which remain stable over several generations and are not predictably affected by seasonal variation in temperature or humidity. This stability in nest microbiome is likely due to social transmission, whereas drift-like processes during new nest foundations explain variation in host microbiomes between nests. This is supported by the lack of obligate symbionts (i.e. no symbionts are present in all spider individuals). Quantitative PCR analyses showed that the bacterial load of individual spiders is stable in healthy nests but can increase dramatically in perishing nests. These increases are not driven by specific bacterial taxa but likely caused by loss of host immune control under deteriorating conditions. Spider nests show an annual survival rate of approximately 45%, but nest death is not correlated to microbiome composition, and the bacteria found in S. dumicola are not considered to be high virulence pathogens.

Metabolite Profiling of the Social Spider Stegodyphus dumicola Along a Climate Gradient

“…Our results provide no evidence for a role of specific symbionts in shaping the observed metabolite profile pattern. The microbiomes of the S. dumicola spiders sampled along the climatic gradient showed no significant population-specific pattern (Figure 2), which is consistent with previous studies of S. dumicola spiders collected over even larger geographic distances (Busck et al, 2020(Busck et al, , 2022. The bacterial genera that dominated S. dumicola's microbiome in this study are identical to those previously found (Borrelia, Diplorickettsia, and Mycoplasma), and are so far not known to provide or enhance thermal tolerance in hosts.…”

“…Comparably, bacterial symbionts in the Asian citrus psyllid (Diaphorina citri) degrade during heat stress due to increased lysosomal activity, which provides nutrients to the surviving symbionts and host (Dossi et al, 2018). Busck et al (2022) estimated that for every host cell there are 1-2 bacterial cells in S. dumicola, and such a bacterial load could potentially influence the host metabolome upon cell lysis and supply the spider host with metabolites aiding its temperature response. Thus, S. dumicola with its microbiome may represent a parallel system to aphids and D. citri, where the microbial symbionts contribute to the host temperature response via cell lysis.…”

Adapting to climate with limited genetic diversity: Nucleotide,DNAmethylation and microbiome variation among populations of the social spiderStegodyphus dumicola

“…The spider microbiome was dominated by Mycoplasma, Diplorickettsia, Borrelia and Weeksellaceae (Figure S5), corroborating a previous study in Stegodyphus dumicola (Busck et al, 2020(Busck et al, , 2022.…”

“…Several aspects of precipitation associated more than expected with relative abundance of bacterial symbionts (Figure 6). A previous study showed an association between high precipitation and microbiome composition (Busck et al, 2022), and together these studies indicate that the microbiome composition of S. dumicola is shaped by aspects of humidity. This association is driven by 10 ASVs from different taxonomic groups that correlate strongly and/or significantly with aspects of precipitation (Figure S17).…”

“…We know from preliminary data that bacteria are not vertically but rather socially transmitted among nest mates in S. dumicola (our unpublished data). Within nests, the microbiome composition does not change much across generations, suggesting relatively high transmission fidelity within nests (Busck et al, 2022), but nests within a population often carry substantially different microbiome compositions (Busck et al, 2020(Busck et al, , 2022.…”