Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution

Liang Shen,Ninglian Wang,Yongqin Liu,Michelle A Allen,Ricardo Cavicchioli,Qing Liu,Yuguang Zhou,Timothy J Williams,Feng Wang,Baiqing Xu

doi:10.1186/s40168-021-01084-z

Abstract

BackgroundMicroorganisms drive critical global biogeochemical cycles and dominate the biomass in Earth’s expansive cold biosphere. Determining the genomic traits that enable psychrophiles to grow in cold environments informs about their physiology and adaptive responses. However, defining important genomic traits of psychrophiles has proven difficult, with the ability to extrapolate genomic knowledge to environmental relevance proving even more difficult.ResultsHere we examined the bacterial genus Arthrobacter and, assisted by genome sequences of new Tibetan Plateau isolates, defined a new clade, Group C, that represents isolates from polar and alpine environments. Group C had a superior ability to grow at −1°C and possessed genome G+C content, amino acid composition, predicted protein stability, and functional capacities (e.g., sulfur metabolism and mycothiol biosynthesis) that distinguished it from non-polar or alpine Group A Arthrobacter. Interrogation of nearly 1000 metagenomes identified an over-representation of Group C in Canadian permafrost communities from a simulated spring-thaw experiment, indicative of niche adaptation, and an under-representation of Group A in all polar and alpine samples, indicative of a general response to environmental temperature.ConclusionThe findings illustrate a capacity to define genomic markers of specific taxa that potentially have value for environmental monitoring of cold environments, including environmental change arising from anthropogenic impact. More broadly, the study illustrates the challenges involved in extrapolating from genomic and physiological data to an environmental setting.AikJUfGrEhgWMtLNAXyFSoVideo

Highlights

Microorganisms drive critical global biogeochemical cycles and dominate the biomass in Earth’s expansive cold biosphere
Phylogenomics To increase the number of Arthrobacter genomes from polar and alpine (PA) environments, a total of 16 isolates from seven lakes, two glaciers, and one wetland on the Tibetan Plateau (Additional file 1: Fig. S1 and Table S1) were sequenced
Our study commenced with the analysis of genome sequences of new Group C Arthrobacter isolated from the Tibetan Plateau and progressed through to a rationalization of Group C abundance in global metagenomes

Summary

Introduction

Microorganisms drive critical global biogeochemical cycles and dominate the biomass in Earth’s expansive cold biosphere. Certain environmental factors can limit or prevent the growth of microorganisms, while enhancing, or being essential for others, resulting in ecological niches that support specific microbiome structures [1]. This phenomenon is well illustrated by a Winogradsky column where light and oxygen can be seen to exert major influences on the diversity and the dynamic of microorganisms throughout its length [2]. There is a growing realization that microorganisms constitute the life support system of the biosphere and must be properly accounted for when devising strategies to mitigate the impacts of human activity on the natural world [5]. We are living in a period in history when the need for society to learn about microbial responses to natural and anthropogenic influences is of unprecedented relevance [5,6,7]

Methods

Results

Discussion

Conclusion