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.

Keywords: Functional redundancy; Heat stress; Ixodes scapularis; Keystone bacteria; Microbial networks; Microbiome.