Ixodes scapularis does not harbor a stable midgut microbiome

Abstract

Hard ticks of the order Ixodidae serve as vectors for numerous human pathogens, including the causative agent of Lyme Disease Borrelia burgdorferi. Tick-associated microbes can influence pathogen colonization, offering the potential to inhibit disease transmission through engineering of the tick microbiota. Here, we investigate whether B. burgdorferi encounters abundant bacteria within the midgut of wild adult Ixodes scapularis, its primary vector. Through the use of controlled sequencing methods and confocal microscopy, we find that the majority of field-collected adult I. scapularis harbor limited internal microbial communities that are dominated by endosymbionts. A minority of I. scapularis ticks harbor abundant midgut bacteria and lack B. burgdorferi. We find that the lack of a stable resident midgut microbiota is not restricted to I. scapularis since extension of our studies to I. pacificus, Amblyomma maculatum, and Dermacentor spp showed similar patterns. Finally, bioinformatic examination of the B. burgdorferi genome revealed the absence of genes encoding known interbacterial interaction pathways, a feature unique to the Borrelia genus within the phylum Spirochaetes. Our results suggest that reduced selective pressure from limited microbial populations within ticks may have facilitated the evolutionary loss of genes encoding interbacterial competition pathways from Borrelia.

Drivers and patterns of microbial community assembly in a Lyme disease vector

“…Specifically, the average I. pacificus microbiome contained only 7 OTUs and was numerically dominated by the endosymbiont, Rickettsia. This finding is consistent with recent work combining direct microbial visualization of I. pacificus 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, 2014Zolnik et al, 2016). While variation in microbial richness observed across studies may be due to differences in the precise species or life stages examined Van Treuren et al, 2015), the difference in OTU richness in our study and those aforementioned is orders of magnitude greater than that typically generated by species-and life stage-specific differences.…”

“…this Rickettsia phylotype has the demonstrated capability of synthesizing folate (Hunter et al, 2015), an essential vitamin absent from the ticks' blood-based diet and which ticks lack the genetic capacity to synthesize de novo (Hill & Wikel, 2005 and Enterobacteriaceae may limit pathogen colonization in Ixodes (Ross et al, 2018), these microbes are not reliably vertically transmitted, and their ability to persist in the tick during a molting event is unknown. Endosymbionts such as Rickettsia, however, are efficiently vertically transmitted and have been associated with reductions in pathogen acquisition in some tick-borne pathogen systems (Gall et al, 2016;Macaluso et al, 2002;Telford, 2009).…”

Sharing the Ride: Ixodes scapularis Symbionts and Their Interactions

“…Characterizing the biological interactions between symbionts and the host tick may illuminate new strategies to prevent tick-borne diseases by inhibiting pathogen colonization of I. scapularis or for engineering paratransgenic organisms antagonistic to pathogens. Studies suggest that some microbes may be excluded from I. scapularis by the presence of others (Steiner et al, 2008;Narasimhan et al, 2014;Ross et al, 2018) and acquisition of a paratransgenic bacterium has been demonstrated for the hard tick Hyalomma dromedarii (Koosha et al, 2019).…”

“…Less clear than the diversity of organisms, is the extent, if any, to which some of these microbes may interact with each other, either directly or indirectly. The published studies in this area are largely limited to predicted interactions based on cooccurrences of two or more organisms in the same tick (Cross et al, 2018;Ross et al, 2018). This review will focus on both the composition of the I. scapularis microbiome and the potential microbial interactions occurring within this tick species.…”

Peer Review #3 of "Bacterial microbiota composition of Ixodes ricinus ticks: the role of environmental variation, tick characteristics and microbial interactions (v0.1)"

“…In contrast, individual tick ID explained over 60% of the variation in microbiota composition. This substantial microbiota variation across individual ticks may be partly explained by some of the bacteria present in ticks being non-resident (i.e., bacteria that were by chance obtained from the environment through the mouth, the anal pore or spiracles or during blood-feeding; Horner-Devine and Bohannan 2006; Engel and Moran 2013;Zolnik et al 2016Zolnik et al , 2018Ross et al 2018). Indeed, there has been a debate whether ticks have a stable microbiota (Ross et al 2018), mirroring the wider debate on how common resident microbiota is in arthropod hosts (Hammer et al 2017).…”