Pan-Genome Portrait of Bacillus mycoides Provides Insights into the Species Ecology and Evolution.

Krzysztof Fiedoruk,Jacques Mahillon,Izabela Swiecicka,Monika Zambrzycka,Justyna M. Drewnowska,Jeffrey A. Gralnick

doi:10.1128/spectrum.00311-21

Krzysztof Fiedoruk, Jacques Mahillon + Show 4 more

Open Access

https://doi.org/10.1128/spectrum.00311-21

Copy DOI

Abstract

ABSTRACTBacillus mycoides is poorly known despite its frequent occurrence in a wide variety of environments. To provide direct insight into its ecology and evolutionary history, a comparative investigation of the species pan-genome and the functional gene categorization of 35 isolates obtained from soil samples from northeastern Poland was performed. The pan-genome of these isolates is composed of 20,175 genes and is characterized by a strong predominance of adaptive genes (∼83%), a significant amount of plasmid genes (∼37%), and a great contribution of prophages and insertion sequences. The pan-genome structure and phylodynamic studies had suggested a wide genomic diversity among the isolates, but no correlation between lineages and the bacillus origin was found. Nevertheless, the two B. mycoides populations, one from Białowieża National Park, the last European natural primeval forest with soil classified as organic, and the second from mineral soil samples taken in a farm in Jasienówka, a place with strong anthropogenic pressure, differ significantly in the frequency of genes encoding proteins enabling bacillus adaptation to specific stress conditions and production of a set of compounds, thus facilitating their colonization of various ecological niches. Furthermore, differences in the prevalence of essential stress sigma factors might be an important trail of this process. Due to these numerous adaptive genes, B. mycoides is able to quickly adapt to changing environmental conditions.IMPORTANCE This research allows deeper understanding of the genetic organization of natural bacterial populations, specifically, Bacillus mycoides, a psychrotrophic member of the Bacillus cereus group that is widely distributed worldwide, especially in areas with continental cold climates. These thorough analyses made it possible to describe, for the first time, the B. mycoides pan-genome, phylogenetic relationship within this species, and the mechanisms behind the species ecology and evolutionary history. Our study indicates a set of functional properties and adaptive genes, in particular, those encoding sigma factors, associated with B. mycoides acclimatization to specific ecological niches and changing environmental conditions.

Highlights

Bacillus mycoides is poorly known despite its frequent occurrence in a wide variety of environments
With regard to psychrotrophic species, while B. wiedmannii belongs to phylogroup II, B. mycoides constitutes phylogroup VI in the scheme proposed by Drewnowska et al [7] and Guinebretière et al [15]
Twenty-one originated from Białowiez_a National Park (BPN), the last European natural primeval forest under protection of World Heritage as a biosphere reserve and with soil classified as organic, while 14 strains were from mineral soil samples taken from a farm in Jasienówka (JAS), a place with strong anthropogenic pressure

Summary

Introduction

Bacillus mycoides is poorly known despite its frequent occurrence in a wide variety of environments. IMPORTANCE This research allows deeper understanding of the genetic organization of natural bacterial populations, Bacillus mycoides, a psychrotrophic member of the Bacillus cereus group that is widely distributed worldwide, especially in areas with continental cold climates These thorough analyses made it possible to describe, for the first time, the B. mycoides pan-genome, phylogenetic relationship within this species, and the mechanisms behind the species ecology and evolutionary history. Psychrotolerance and specific sequences in the 16S rRNA genes and cspA genes did not properly distinguish B. weihenstephanensis from some other B. cereus sensu lato [14] Based on this reclassification, in this work, we consider as B. mycoides both the isolates of rhizoidal colonies and those forming regular colonies, which have the ability to grow at temperatures ranging from 5 to 40°C. With regard to psychrotrophic species, while B. wiedmannii belongs to phylogroup II, B. mycoides (together with former B. weihenstephanensis) constitutes phylogroup VI in the scheme proposed by Drewnowska et al [7] and Guinebretière et al [15]

Methods

Results

Conclusion