Abstract
Vector‐borne diseases constitute a major global health burden and are increasing in geographic range and prevalence. Mounting evidence has demonstrated that the vector microbiome can impact pathogen dynamics, making the microbiome a focal point in vector‐borne disease ecology. However, efforts to generalize preliminary findings across studies and systems and translate these findings into disease control strategies are hindered by a lack of fundamental understanding of the processes shaping the vector microbiome and the interactions therein. Here, we use 16S rRNA sequencing and apply a community ecology framework to analyze microbiome community assembly and interactions in Ixodes pacificus, the Lyme disease vector in the western United States. We find that vertical transmission routes drive population‐level patterns in I. pacificus microbial diversity and composition, but that microbial function and overall abundance do not vary over time or between clutches. Further, we find that the I. pacificus microbiome is not strongly structured based on competition but assembles nonrandomly, potentially due to vector‐specific filtering processes which largely eliminate all but the dominant endosymbiont, Rickettsia. At the scale of the individual I. pacificus, we find support for a highly limited internal microbial community, and hypothesize that the tick endosymbiont may be the most important component of the vector microbiome in influencing pathogen dynamics.
Highlights
| MATERIALS AND METHODSAdult female I. pacificus were field‐collected from China Camp State Park in Marin County, CA, and fed to repletion on New Zealand white rabbits in the laboratory
We examined the process of community assembly in the initial, posthatching I. pacificus microbiome, and found individual ticks to harbor a depauperate microbial community
The average I. pacificus microbiome contained only 7 operational taxonomic units (OTUs) and was numerically dominated by the endosymbiont, Rickettsia. This finding is consistent with recent work combining direct microbial visualization of I. pa‐ cificus with sequencing methods (Ross et al, 2018), but contradicts previous reports indicating that Ixodid ticks harbor highly diverse microbiomes, including hundreds to thousands of OTUs (Andreotti et al, 2011; Budachetri et al, 2014; Carpi et al, 2011; Estrada‐Peña, Cabezas‐Cruz, Pollet, Vayssier‐Taussat, & Cosson, 2018; Nakao et al, 2013; Ponnusamy et al, 2014; Fryxell & DeBruyn, 2016; Rynkiewicz et al, 2015, Zhang et al, 2014; Zolnik et al, 2016)
Summary
Adult female I. pacificus were field‐collected from China Camp State Park in Marin County, CA, and fed to repletion on New Zealand white rabbits in the laboratory. Comparing across environmental exposure groups, we observed a significant decrease in species evenness, Shannon's diversity, and Faith's phylogenetic diversity over time (ANOVA F = 3.32, 3.02, 4.0, df = 3, p = 0.026, 0.037, 0.012) (Figure 3 and Appendix Figure S3), but no difference in species richness (ANOVA F = 1.61; df = 3; p = 0.20). The observed checkerboard score, an index measuring the number of species which never co‐occur, was significantly lower than that of the simulated communities, indicating that there were fewer nega‐ tive interactions among OTUs than expected by chance (Stone & Roberts, 1992) This result was upheld for OTUs aggregated at both the genus and phylum level (Z = −6.59, −7.17; p < 0.001), enabling us to reject the null hypothesis of neutral assortment The estimated functional gene content of the I. pacificus microbiome did not vary by treatment, despite differences in species composition and diversity
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