Ixodes scapularisdoes not harbor a stable midgut microbiome

Abstract

1Hard ticks of the order Ixodidae serve as vectors for numerous human pathogens, including the 2 causative agent of Lyme Disease Borrelia burgdorferi. Tick-associated microbes can influence 3 pathogen colonization, offering the potential to inhibit disease transmission through engineering 4 of the tick microbiota. Here, we investigate whether B. burgdorferi encounters abundant bacteria 5 within the midgut of wild adult Ixodes scapularis, its primary vector. Through the use of 6 controlled sequencing methods and confocal microscopy, we find that the majority of field-7 collected adult I. scapularis harbor limited internal microbial communities that are dominated by 8 endosymbionts. A minority of I. scapularis ticks harbor abundant midgut bacteria and lack B. 9 burgdorferi. We find that the lack of a stable resident midgut microbiota is not restricted to I. 10 scapularis since extension of our studies to I. pacificus, Amblyomma maculatum, and 11Dermacentor spp showed similar patterns. Finally, bioinformatic examination of the B. 12 burgdorferi genome revealed the absence of genes encoding known interbacterial interaction 13 pathways, a feature unique to the Borrelia genus within the phylum Spirochaetes. Our results 14 suggest that reduced selective pressure from limited microbial populations within ticks may have 15 facilitated the evolutionary loss of genes encoding interbacterial competition pathways from 16Borrelia.

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, ), but contradicts previous reports indicating that Ixodid ticks harbor highly diverse microbiomes, including hundreds to thousands of OTUs (Andreotti et al, ; Budachetri et al, ; Carpi et al, ; Estrada‐Peña, Cabezas‐Cruz, Pollet, Vayssier‐Taussat, & Cosson, ; Nakao et al, ; Ponnusamy et al, ; Fryxell & DeBruyn, ; Rynkiewicz et al, , Zhang et al, ; Zolnik et al, ). While variation in microbial richness observed across studies may be due to differences in the precise species or life stages examined (Kwan et al, ; Van Treuren et al, ), 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.…”

“…The presence of a depauperate microbiome, and the dominance of specific, beneficial microbes, highlights the need to determine the role of tick endosymbionts in pathogen transmission. While other environmentally acquired microbes such as Bacillus, Pseudomonas, and Enterobacteriaceae may limit pathogen colonization in Ixodes (Ross et al, ), 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, ; Macaluso et al, ; Telford, ).…”

Are you what you eat? A highly transient and prey‐influenced gut microbiome in the grey house spider Badumna longinqua

“…Current work on the arthropod gut microbiome yields contradictory results, finding host‐microbial interactions of widely varying levels of intimacy in different taxa. Some studies suggest a great functional importance of gut microbes for their arthropod hosts, leading to a stable and predictable microbial community (Chu, Spencer, Curzi, Zavala, & Seufferheld, ; Engel & Moran, ; Reese & Dunn, ; Ruokolainen, Ikonen, Makkonen, & Hanski, ; Russell et al, ; Sanders et al, ), whereas other work highlights the instability and transient nature of arthropod gut ecosystems (Engel & Moran, ; Ross et al, ). The often simple structure of arthropod guts and associated short transit times of ingested material can make them a highly unpredictable environment for microbial colonizers (Paniagua Voirol, Frago, Kaltenpoth, Hilker, & Fatouros, ).…”

Contrasting Strategies: Human Eukaryotic Versus Bacterial Microbiome Research

“…, ; Ross et al. ). Recognizing this issue earlier in the development of eukaryotic microbiome research may allow more fine‐grained ecological and evolutionary insight into microbiota dynamics.…”

“…A few interesting exceptions include David et al (2014), who detected many foodborne bacteria and fungi (some of which expressed genes), and Minot et al (2011), who took transience into account for viruses in the gut. It is now better recognized that numerous insects do not have resident bacterial microbiota, and that this has important implications for bacterial community stability, host fitness and mutualism (Hammer et al 2017(Hammer et al , 2019Ross et al 2018). Recognizing this issue earlier in the development of eukaryotic microbiome research may allow more fine-grained ecological and evolutionary insight into microbiota dynamics.…”