The early events underlying genome evolution in a localized Sinorhizobium meliloti population

Abstract

BackgroundPopulation genetic analyses based on genome-wide sequencing data have been carried out for Sinorhizobium medicae and S. meliloti, two closely related bacterial species forming nitrogen-fixing symbioses with plants of the genus Medicago. However, genome coverage was low or the isolates had a broad geographic distribution, making it difficult to interpret the estimated diversity and to unravel the early events underlying population genetic variations and ecological differentiation.ResultsHere, to gain insight into the early genome level variation and diversification within S. meliloti populations, we first used Illumina paired-end reads technology to sequence a new clone of S. meliloti strain GR4, a highly competitive strain for alfalfa nodulation. The Illumina data and the GR4 genome sequence previously obtained with 454 technology were used to generate a high-quality reference genome sequence. We then used Illumina technology to sequence the genomes of 13 S. meliloti isolates representative of the genomic variation within the GR4-type population, obtained from a single field site with a high degree of coverage. The genome sequences obtained were analyzed to determine nucleotide diversity, divergence times, polymorphism and genomic variation. Similar low levels of nucleotide diversity were observed for the chromosome, pSymB and pSymA replicons. The isolates displayed other types of variation, such as indels, recombination events, genomic island excision and the transposition of mobile elements.ConclusionsOur results suggest that the GR4-type population has experienced a process of demographic expansion and behaves as a stable genotypic cluster of genome-wide similarity, with most of the genome following a clonal pattern of evolution. Although some of genetic variation detected within the GR4-type population is probably due to genetic drift, others might be important in diversification and environmental adaptation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2878-9) contains supplementary material, which is available to authorized users.

The underlying process of early ecological and genetic differentiation in a facultative mutualistic Sinorhizobium meliloti population

“…Genome sequencing data of 13 of these GR4-type isolates (3G48, 3D13, 3F11, 7D33, 5G35, 5F20, 7G54, 2B2, 1A66, 7A75, 5D25, 1B5 and 2A8, referred to as G1 to G13, respectively) were reported previously 22 .…”

“…The low frequency of the GID and the low level of diversity throughout the genome in this population suggest that the GID was acquired recently, by recombination, rather than being a remnant from ancient clonal frame divergence.

Figure 1Genealogy of the 21 isolates representative of genomic variation within the S. meliloti GR4-type population. The maximum clade credibility tree was estimated with BEAST 2 25 , from the alignment (Supplementary Data 1) of concatenated genes carrying SNPs from the chromosome, pSymB and pSymA replicons (280,068 nts) of all isolates, as previously determined within the GR4-type population 22 . Node bars indicate the 95% credibility intervals (95% HPD) for node age, and posterior probabilities (>0.5) are indicated (in italics) on the branches.

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Contribution of Mobile Group II Introns to Sinorhizobium meliloti Genome Evolution

“…The intron is able to recognize this target site because this gene carries IBS sequences similar to those of IS Rm2011-2 . Following the sequencing of the genome of GR4 ( Martínez-Abarca et al, 2013 ), oxi1 was identified in pRmeGR4d (pSymB) as a gene encoding an oxidoreductase (WP_010975806.1), resulting from an ectopic transposition event that has occurred independently several times in the natural population ( Toro et al, 2016 ). In the GR4-type population analyzed, 4.1% of the isolates displayed such intron insertions, but this variant is fixed in 95% of EM2-type isolates, a different population obtained from nodules also occupied by GR4-type strains, suggesting that it may be subject to selective pressure ( Muñoz et al, 2001 ).…”

“…In the GR4-type population analyzed, 4.1% of the isolates displayed such intron insertions, but this variant is fixed in 95% of EM2-type isolates, a different population obtained from nodules also occupied by GR4-type strains, suggesting that it may be subject to selective pressure ( Muñoz et al, 2001 ). Moreover, whole-genome sequencing in GR4-type isolates identified another ectopic site, an intron insertion in a gene encoding a NAD(P)-dependent oxidoreductase (WP_010969452.1), corresponding to an event that probably occurred about 1700 years ago ( Toro et al, 2016 , 2017 ). The biological significance of the targeting of these genes by RmInt1 in S. meliloti is unknown.…”

“…Whole-genome sequence analyses have been performed for S. meliloti and S. medicae ( Bailly et al, 2011 ; Galardini et al, 2011 , 2013 ; Epstein et al, 2012 ; Sugawara et al, 2013 ), and some studies have indicated that the pSymB megaplasmid plays a key role in intraspecies differentiation ( Galardini et al, 2013 , 2015 ). Whole-genome sequencing of isolates from a natural S. meliloti population (GR4-type) isolated from M. sativa (alfalfa) root nodules revealed the existence of genotypic variation underlying early genetic and ecological differentiation ( Toro et al, 2016 , 2017 ). In addition to the small numbers of single-nucleotide polymorphisms uniformly distributed over the multipartite genome, the isolates analyzed exhibited other types of genomic variation, indels of various sizes, some recombination events including the excision and acquisition of genomic islands, and the transposition of mobile elements, which seem to be the early microevolutionary forces influencing this multipartite genome.…”