Thermostable Keystone Bacteria Maintain the Functional Diversity of the Ixodes scapularis Microbiome Under Heat Stress

Abstract

Variations in the composition and diversity of tick microbiome due to high temperatures may influence the hierarchy of community members as a response to environmental change. Modifications in the community structure are hypothesized to drive alterations in the presence and/or abundance of functional pathways in the bacterial metagenome. In this study, this hypothesis was tested by using published 16S rRNA datasets of Ixodes scapularis males incubated at different temperatures (i.e., 4, 20, 30, and 37 °C) in a laboratory setting. Changes in community structure and functional profiles in response to temperature shifts were measured using co-occurrence networks and metagenome inference. Results from laboratory-reared ticks were then compared with those of field-collected ticks. The results from laboratory-reared ticks showed that high temperature altered the structure of the microbial community and decreased the number of keystone taxa. Notably, four taxa were identified as keystone in all the temperatures, and the functional diversity of the tick microbiome was contained in the four thermostable keystone their associated bacterial taxa. Three of the thermostable keystone taxa were also found in free-living ticks collected in Massachusetts. Moreover, the comparison of functional profiles of laboratory-reared and field-collected ticks revealed the existence of an important set of metabolic pathways that were common among the different datasets. Similar to the laboratory-reared ticks, the keystone taxa identified in field-collected ticks alongside their consortia (co-occurring taxa) were sufficient to retain the majority of the metabolic pathways in the functional profile. These results suggest that keystone taxa are essential in the stability and the functional resiliency of the tick microbiome under heat stress.

Rickettsial pathogens drive microbiota assembly in Hyalomma marginatum and Rhipicephalus bursa ticks

“…Keystone taxa are known to have a major influence on the structure and function of microbiota at specific spatial or temporal contexts (Banerjee et al, 2018; Wu‐Chuang, Obregon, Mateos‐Hernández, et al, 2022). Certain keystone bacteria have been associated with the recovery of human gut microbiota after antibiotic exposure (Gibbons, 2020), and in another study, four keystone bacteria were found to maintain the functional diversity of the I. scapularis microbiota under intense heat stress (Wu‐Chuang et al, 2021; Wu‐Chuang, Obregon, Estrada‐Peña, et al, 2022). Through the privileged connectivity to keystone taxa in H. marginatum bacterial microbiota, Rickettsia may exert an influence microbial community assembly and resiliency to attack (i.e.…”

“…Ticks have intricate ecological interactions with microorganisms present in their microbiota (Wu‐Chuang et al, 2021; Wu‐Chuang, Obregon, Estrada‐Peña, et al, 2022). Some of these microorganisms are considered human pathogens, such as Rickettsia sibirica mongolitimonae (Jakimovski et al, 2022).…”

“…Some of these microorganisms are considered human pathogens, such as Rickettsia sibirica mongolitimonae (Jakimovski et al, 2022). Ticks also harbour endosymbionts like Coxiella ‐like (Zhong, 2012) or Francisella ‐like endosymbionts (Duron et al, 2018), as well as commensal bacteria (Wu‐Chuang et al, 2021; Wu‐Chuang, Obregon, Estrada‐Peña, et al, 2022). While the distinction between human pathogens and other non‐pathogenic microorganisms carried by ticks is still being investigated, it is possible to differentiate between obligate tick endosymbionts, which are vertically transmitted from mother to offspring and mainly reside in vector reproductive organs, and commensal bacteria, which are horizontally acquired and heavily influenced by the ecological conditions in which ticks are found (Hussain et al, 2022; Wu‐Chuang et al, 2021; Wu‐Chuang, Obregon, Estrada‐Peña, et al, 2022).…”

“…salivary glands) and external (e.g. cuticle) tick tissues, referred here as bacterial microbiota (Wu‐Chuang et al, 2021; Wu‐Chuang, Obregon, Estrada‐Peña, et al, 2022), is a dynamic entity that can be directly or indirectly influenced by biotic factors like pathogen infections (Maitre, Wu‐Chuang, Aželytė, et al, 2022; Maitre, Wu‐Chuang, Mateos‐Hernández, et al, 2022) or abiotic factors like temperature (Thapa et al, 2019; Wu‐Chuang et al, 2021; Wu‐Chuang, Obregon, Estrada‐Peña, et al, 2022).…”

The Symbiotic Continuum Within Ticks: Opportunities for Disease Control

“…For example, the microbiome of I. scapularis larvae and nymphs shared 80 taxa (24.6%, total 324), while out of 342 predicted metabolic pathways, 82.7%, were shared by all the tick samples ( Estrada-Peña et al, 2020a ). Furthermore, the I. scapularis microbiota exposed to pathogen infection, antimicrobial peptide or anti-tick host immunity shared a very reduced taxonomic core of 61 bacterial genera (7.4%, total 821), while the majority (i.e., 381) of the metabolic pathways (87.2%, total 437) were identified in all the samples ( Estrada-Peña et al, 2020b ), Also, despite high temperature altered the structure of the microbial community in I. scapularis ( Thapa et al, 2019 ; Wu-Chuang et al, 2021b ) four keystone taxa found across the temperature gradient, and their directly connected neighbors, contributed to more than 99% of the predicted pathways regardless the incubation temperature ( Wu-Chuang et al, 2021b ). This suggests that the tick microbiome is a stable source of metabolic functions with potential implications for tick physiology.…”