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Adaptation in Toxic Environments: Arsenic Genomic Islands in the Bacterial Genus Thiomonas.

Freel KC, Krueger MC, Farasin J, Brochier-Armanet C, Barbe V, Andrès J, Cholley PE, Dillies MA, Jagla B, Koechler S, Leva Y, Magdelenat G, Plewniak F, Proux C, Coppée JY, Bertin PN, Heipieper HJ, Arsène-Ploetze F - PLoS ONE (2015)

Bottom Line: CB2 genome revealed various rearrangements had occurred in comparison to what was observed in 3As and K12 and over 20 genomic islands (GEIs) were found in each of these three genomes.We performed a detailed comparison of the two arsenic-related islands found in CB2, carrying the genes required for arsenite oxidation and As resistance, with those found in K12, 3As, and five other Thiomonas strains also isolated from Carnoulès (CB1, CB3, CB6, ACO3 and ACO7).Our results suggest that these arsenic-related islands have evolved differentially in these closely related Thiomonas strains, leading to divergent capacities to survive in As rich environments.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire Génétique Moléculaire, Génomique et Microbiologie, UMR7156, CNRS-Université de Strasbourg, Département Microorganismes, Génomes, Environnement, Equipe Ecophysiologie Moléculaire des Microorganismes, Institut de Botanique, Strasbourg, France.

ABSTRACT
Acid mine drainage (AMD) is a highly toxic environment for most living organisms due to the presence of many lethal elements including arsenic (As). Thiomonas (Tm.) bacteria are found ubiquitously in AMD and can withstand these extreme conditions, in part because they are able to oxidize arsenite. In order to further improve our knowledge concerning the adaptive capacities of these bacteria, we sequenced and assembled the genome of six isolates derived from the Carnoulès AMD, and compared them to the genomes of Tm. arsenitoxydans 3As (isolated from the same site) and Tm. intermedia K12 (isolated from a sewage pipe). A detailed analysis of the Tm. sp. CB2 genome revealed various rearrangements had occurred in comparison to what was observed in 3As and K12 and over 20 genomic islands (GEIs) were found in each of these three genomes. We performed a detailed comparison of the two arsenic-related islands found in CB2, carrying the genes required for arsenite oxidation and As resistance, with those found in K12, 3As, and five other Thiomonas strains also isolated from Carnoulès (CB1, CB3, CB6, ACO3 and ACO7). Our results suggest that these arsenic-related islands have evolved differentially in these closely related Thiomonas strains, leading to divergent capacities to survive in As rich environments.

No MeSH data available.


Related in: MedlinePlus

Comparison among the CB2, K12, and 3As genomes.(A) Dot plot, CB2 vs 3As and 3As vs K12. The genomes of 3As and K12 are well conserved while the CB2 genome appears to have undergone chromosomal rearrangements. (B) Scheme demonstrating the key differences between the Thiomonas ancestor and CB2 genome. Above, “1”, “2” and “3” highlight a translocation of 0.1 Mb, an inversion of 1.8 Mb and a translocation and inversion of 0.13 Mb, respectively.
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pone.0139011.g002: Comparison among the CB2, K12, and 3As genomes.(A) Dot plot, CB2 vs 3As and 3As vs K12. The genomes of 3As and K12 are well conserved while the CB2 genome appears to have undergone chromosomal rearrangements. (B) Scheme demonstrating the key differences between the Thiomonas ancestor and CB2 genome. Above, “1”, “2” and “3” highlight a translocation of 0.1 Mb, an inversion of 1.8 Mb and a translocation and inversion of 0.13 Mb, respectively.

Mentions: Previous analysis based on the use of CGH revealed dramatic variation in the genomic content of eight Thiomonas strains (CB1, CB2, CB3, CB6, 3As, Tm. arsenivorans, Ynys1 and Tm. perometabolis) despite their phylogenetic proximity. Indeed, the 16S rDNA/rpoA-based phylogeny of the CB1, CB2, CB3, CB6, and 3As isolates (which share a 97% nucleotide identity), as well as DNA-DNA hybridization experiments, suggested that while they are indeed 5 different strains, they are of the same species. However, subtle physiological differences were observed among the isolates, and only 74.7% of the genome of strain 3As was sufficiently conserved to allow hybridization using the CGH approach [16]. Nevertheless, this did not allow for the comparison of genomic synteny or to detect if the genomes shared similar architectures. Here, due to the high quality of sequence assembly, the architecture of the 3As, K12 and CB2 genomes could be compared and the genomic islands identified. Dot plots were constructed for pairwise genomic comparisons among the three isolates, revealing striking similarities between 3As and K12 compared to the CB2 genome (Fig 2A). The 3As and K12 genomes are highly syntenic and similar in gene content (Fig 2A), although 3As harbors several insertions (indicated by breaks in the line) and one inversion compared to K12. In contrast, genome organization between CB2 and 3As is not well conserved due to a variety of rearrangements and inversions (Fig 2A). Since the 3As and K12 strains are phylogenetically distant but harbor similar genomic organization (Figs 1 and 2A), we hypothesize that these genomes represent the ancestral state, while that of CB2 is more derived (Fig 2B). Accordingly, three major genomic rearrangements and inversions could have occurred in the CB2 lineage after its divergence from the two others strains: (i) the translocation of a 0.1 Mb region; (ii) the inversion of a 1.8 Mb region, and (iii) the translocation and inversion of a 0.13 Mb region (Fig 2B).


Adaptation in Toxic Environments: Arsenic Genomic Islands in the Bacterial Genus Thiomonas.

Freel KC, Krueger MC, Farasin J, Brochier-Armanet C, Barbe V, Andrès J, Cholley PE, Dillies MA, Jagla B, Koechler S, Leva Y, Magdelenat G, Plewniak F, Proux C, Coppée JY, Bertin PN, Heipieper HJ, Arsène-Ploetze F - PLoS ONE (2015)

Comparison among the CB2, K12, and 3As genomes.(A) Dot plot, CB2 vs 3As and 3As vs K12. The genomes of 3As and K12 are well conserved while the CB2 genome appears to have undergone chromosomal rearrangements. (B) Scheme demonstrating the key differences between the Thiomonas ancestor and CB2 genome. Above, “1”, “2” and “3” highlight a translocation of 0.1 Mb, an inversion of 1.8 Mb and a translocation and inversion of 0.13 Mb, respectively.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4589449&req=5

pone.0139011.g002: Comparison among the CB2, K12, and 3As genomes.(A) Dot plot, CB2 vs 3As and 3As vs K12. The genomes of 3As and K12 are well conserved while the CB2 genome appears to have undergone chromosomal rearrangements. (B) Scheme demonstrating the key differences between the Thiomonas ancestor and CB2 genome. Above, “1”, “2” and “3” highlight a translocation of 0.1 Mb, an inversion of 1.8 Mb and a translocation and inversion of 0.13 Mb, respectively.
Mentions: Previous analysis based on the use of CGH revealed dramatic variation in the genomic content of eight Thiomonas strains (CB1, CB2, CB3, CB6, 3As, Tm. arsenivorans, Ynys1 and Tm. perometabolis) despite their phylogenetic proximity. Indeed, the 16S rDNA/rpoA-based phylogeny of the CB1, CB2, CB3, CB6, and 3As isolates (which share a 97% nucleotide identity), as well as DNA-DNA hybridization experiments, suggested that while they are indeed 5 different strains, they are of the same species. However, subtle physiological differences were observed among the isolates, and only 74.7% of the genome of strain 3As was sufficiently conserved to allow hybridization using the CGH approach [16]. Nevertheless, this did not allow for the comparison of genomic synteny or to detect if the genomes shared similar architectures. Here, due to the high quality of sequence assembly, the architecture of the 3As, K12 and CB2 genomes could be compared and the genomic islands identified. Dot plots were constructed for pairwise genomic comparisons among the three isolates, revealing striking similarities between 3As and K12 compared to the CB2 genome (Fig 2A). The 3As and K12 genomes are highly syntenic and similar in gene content (Fig 2A), although 3As harbors several insertions (indicated by breaks in the line) and one inversion compared to K12. In contrast, genome organization between CB2 and 3As is not well conserved due to a variety of rearrangements and inversions (Fig 2A). Since the 3As and K12 strains are phylogenetically distant but harbor similar genomic organization (Figs 1 and 2A), we hypothesize that these genomes represent the ancestral state, while that of CB2 is more derived (Fig 2B). Accordingly, three major genomic rearrangements and inversions could have occurred in the CB2 lineage after its divergence from the two others strains: (i) the translocation of a 0.1 Mb region; (ii) the inversion of a 1.8 Mb region, and (iii) the translocation and inversion of a 0.13 Mb region (Fig 2B).

Bottom Line: CB2 genome revealed various rearrangements had occurred in comparison to what was observed in 3As and K12 and over 20 genomic islands (GEIs) were found in each of these three genomes.We performed a detailed comparison of the two arsenic-related islands found in CB2, carrying the genes required for arsenite oxidation and As resistance, with those found in K12, 3As, and five other Thiomonas strains also isolated from Carnoulès (CB1, CB3, CB6, ACO3 and ACO7).Our results suggest that these arsenic-related islands have evolved differentially in these closely related Thiomonas strains, leading to divergent capacities to survive in As rich environments.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire Génétique Moléculaire, Génomique et Microbiologie, UMR7156, CNRS-Université de Strasbourg, Département Microorganismes, Génomes, Environnement, Equipe Ecophysiologie Moléculaire des Microorganismes, Institut de Botanique, Strasbourg, France.

ABSTRACT
Acid mine drainage (AMD) is a highly toxic environment for most living organisms due to the presence of many lethal elements including arsenic (As). Thiomonas (Tm.) bacteria are found ubiquitously in AMD and can withstand these extreme conditions, in part because they are able to oxidize arsenite. In order to further improve our knowledge concerning the adaptive capacities of these bacteria, we sequenced and assembled the genome of six isolates derived from the Carnoulès AMD, and compared them to the genomes of Tm. arsenitoxydans 3As (isolated from the same site) and Tm. intermedia K12 (isolated from a sewage pipe). A detailed analysis of the Tm. sp. CB2 genome revealed various rearrangements had occurred in comparison to what was observed in 3As and K12 and over 20 genomic islands (GEIs) were found in each of these three genomes. We performed a detailed comparison of the two arsenic-related islands found in CB2, carrying the genes required for arsenite oxidation and As resistance, with those found in K12, 3As, and five other Thiomonas strains also isolated from Carnoulès (CB1, CB3, CB6, ACO3 and ACO7). Our results suggest that these arsenic-related islands have evolved differentially in these closely related Thiomonas strains, leading to divergent capacities to survive in As rich environments.

No MeSH data available.


Related in: MedlinePlus