Repeated horizontal gene transfers triggered parallel evolution of magnetotaxis in two evolutionary divergent lineages of magnetotactic bacteria

Abstract

Under the same selection pressures, two genetically divergent populations may evolve in parallel towards the same adaptive solutions. Here, we hypothesized that magnetotaxis (i.e. magnetically guided chemotaxis) represents a key adaptation to micro-oxic habitats in aquatic sediments and that its parallel evolution homogenised the phenotypes of two evolutionary divergent clusters of freshwater spirilla. All magnetotactic bacteria affiliated to the Magnetospirillum genus (Alphaproteobacteria class) biomineralize the same magnetic particle chains and share highly similar physiological and ultrastructural features. We looked for the processes that could have contributed at shaping such an evolutionary pattern by reconciling species and gene trees using newly sequenced genomes of Magnetospirillum related bacteria. We showed that repeated horizontal gene transfers and homologous recombination of entire operons contributed to the parallel evolution of magnetotaxis. We propose that such processes could represent a more parsimonious and rapid solution for adaptation compared to independent and repeated de novo mutations, especially in the case of traits as complex as magnetotaxis involving tens of interacting proteins. Besides strengthening the idea about the importance of such a function in microoxic habitats, these results reinforce previous observations in experimental evolution suggesting that gene flow could alleviate clonal interference and speed up adaptation under some circumstances.

Diverse Intracellular Inclusion Types Within Magnetotactic Bacteria: Implications for Biogeochemical Cycling in Aquatic Environments

“…Phylogenetic analysis based on 16S rRNA gene sequencing demonstrates that strain WYHS‐1 belongs to the Alphaproteobacteria class of the Proteobacteria phylum (Figure 2). Its 16S rRNA gene sequences have low similarity with all known MTB (<95%) and only a 90.1% and 93.9% sequence identity to MTB strains LM‐1 and CCP‐1, respectively (Monteil, Benzerara, et al., 2020; Monteil, Grouzdev, et al., 2020). Therefore, strain WYHS‐1 represents a novel MTB species.…”

A Compass To Boost Navigation: Cell Biology of Bacterial Magnetotaxis

“…Transfer of 32 essential and accessory mam and mms genes from M. gryphiswaldense into the photosynthetic alphaproteobacterium Rhodospirillum rubrum resulted in its "magnetization," that is, it caused the biosynthesis of magneto-somes resembling those of the donor M. gryphiswaldense and demonstrated that these genes are basically sufficient to confer magnetosome biosynthesis to this hithertononmagnetic microbe (32). This also highlights that the genetic equipment to form magnetosomes can be transmitted horizontally (33,34), although magnetotaxis capabilities of the recent MTB mostly seem to descend from a common ancestor (31,35,36).…”

Magnetic flux closure in mutant magnetotactic bacteria elucidates a key signature of magnetofossils

“…They may include gene duplication events 39 , or horizontal gene transfers (i.e. an exchange of genetic material through direct physical interactions between two organisms) 63 . Once the genetic basis of chain configurations is fully understood, the methodology we describe in this work can be used to provide a temporal constrain on evolutionary events that occurred in one of the oldest and more diverse group of biomineralizing organisms.…”