Population Genomics of Microbial Biostalactites: Non-recombinogenic Genome Islands and Microdiversification by Transposons.

Kateřina Burkartová,Lukáš Falteisek,Jakub Rídl,Jiří Dresler

doi:10.3389/fmicb.2022.828531

Abstract

Intrapopulation genetic variability in prokaryotes is receiving increasing attention thanks to improving sequencing methods; however, the ability to distinguish intrapopulation variability from species clusters or initial stages of gene flow barrier development remains insufficient. To overcome this limitation, we took advantage of the lifestyle of Ferrovum myxofaciens, a species that may represent 99% of prokaryotic microbiome of biostalactites growing at acid mine drainage springs. We gained four complete and one draft metagenome-assembled F. myxofaciens genomes using Oxford Nanopore and Illumina sequencing and mapped the reads from each sample on the reference genomes to assess the intrapopulation variability. We observed two phenomena associated with intrapopulation variability: hypervariable regions affected by mobilome expansion called “scrapyards,” and variability in gene disruptions caused by transposons within each population. Both phenomena were previously described in prokaryotes. However, we present here for the first time scrapyard regression and the development of a new one. Nearly complete loss of intrapopulation short sequence variability in the old scrapyard and high variability in the new one suggest that localized gene flow suppression is necessary for scrapyard formation. Concerning the variable gene disruptions, up to 9 out of 41 occurrences per sample were located in highly conserved diguanylate cyclases/phosphodiesterases. We propose that microdiversification of life strategies may be an adaptive outcome of random diguanylate cyclase elimination. The mine biostalactites thus proved as a unique model system for describing genomic intrapopulation processes, as they offer easily sampleable units enriched in a single microbial species.

Highlights

Population genetics was not initially applied to prokaryotic microorganisms since they were assumed as a simple cluster of clonally propagating lineages
Increasing amount of closely related genomes available for a comparison led to revelation of genetically coherent microbial populations, where gene flow between lineages prevents their uncontrolled diversification by random mutations
Based on 16S rDNA amplicon sequencing, 5 mine biostalactites with Ferrovum sp. representing 87.4–99.3% of the microbial communities were selected for metagenome sequencing (Supplementary Table 2)

Summary

Introduction

Population genetics was not initially applied to prokaryotic microorganisms since they were assumed as a simple cluster of clonally propagating lineages. Accumulation of diversifying mutations and occasional genome-wide selective sweeps are the only genetic processes allowed in this model. The genetic promiscuity among distantly related microbes created a picture of prokaryotic evolution as a network rather than tree In this model, genomes could be imagined as transitory associations of phylogenetically diverse genes (e.g., Dagan et al, 2008). Increasing amount of closely related genomes available for a comparison led to revelation of genetically coherent microbial populations, where gene flow between lineages prevents their uncontrolled diversification by random mutations. In these populations, alleles combine freely and selection acts on individual genes instead of genomes in prokaryotes (Whitaker et al, 2005). A single genome-wide selective sweep was observed (Bendall et al, 2016)

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Discussion

Conclusion