Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus

Lillian G. Acuña, Juan Pablo Cárdenas, Paulo C. Covarrubias, Juan José Haristoy, Rodrigo Flores, Harold Nuñez, Gonzalo Riadi, Amir Shmaryahu, Jorge Valdés, Mark Dopson, Douglas E. Rawlings, Jillian F. Banfield, David S. Holmes, Raquel Quatrini

Resultado de la investigación: Article

36 Citas (Scopus)

Resumen

Background: Acidithiobacillus caldus is a sulfur oxidizing extreme acidophile and the only known mesothermophile within the Acidithiobacillales. As such, it is one of the preferred microbes for mineral bioprocessing at moderately high temperatures. In this study, we explore the genomic diversity of A. caldus strains using a combination of bioinformatic and experimental techniques, thus contributing first insights into the elucidation of the species pangenome. Principal Findings: Comparative sequence analysis of A. caldus ATCC 51756 and SM-1 indicate that, despite sharing a conserved and highly syntenic genomic core, both strains have unique gene complements encompassing nearly 20% of their respective genomes. The differential gene complement of each strain is distributed between the chromosomal compartment, one megaplasmid and a variable number of smaller plasmids, and is directly associated to a diverse pool of mobile genetic elements (MGE). These include integrative conjugative and mobilizable elements, genomic islands and insertion sequences. Some of the accessory functions associated to these MGEs have been linked previously to the flexible gene pool in microorganisms inhabiting completely different econiches. Yet, others had not been unambiguously mapped to the flexible gene pool prior to this report and clearly reflect strain-specific adaption to local environmental conditions. Significance: For many years, and because of DNA instability at low pH and recurrent failure to genetically transform acidophilic bacteria, gene transfer in acidic environments was considered negligible. Findings presented herein imply that a more or less conserved pool of actively excising MGEs occurs in the A. caldus population and point to a greater frequency of gene exchange in this econiche than previously recognized. Also, the data suggest that these elements endow the species with capacities to withstand the diverse abiotic and biotic stresses of natural environments, in particular those associated with its extreme econiche.

Idioma originalEnglish
Número de artículoe78237
PublicaciónPLoS ONE
Volumen8
N.º11
DOI
EstadoPublished - 8 nov 2013

Huella dactilar

Acidithiobacillus caldus
Acidithiobacillus
Gene Pool
Genes
Genome
genome
Acidithiobacillales
Interspersed Repetitive Sequences
Genomic Islands
plasmids
complement
genes
Insertional Mutagenesis
bioprocessing
genomic islands
Computational Biology
microorganisms
genomics
Sulfur
Gene Frequency

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Citar esto

Acuña, L. G., Cárdenas, J. P., Covarrubias, P. C., Haristoy, J. J., Flores, R., Nuñez, H., ... Quatrini, R. (2013). Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus. PLoS ONE, 8(11), [e78237]. https://doi.org/10.1371/journal.pone.0078237
Acuña, Lillian G. ; Cárdenas, Juan Pablo ; Covarrubias, Paulo C. ; Haristoy, Juan José ; Flores, Rodrigo ; Nuñez, Harold ; Riadi, Gonzalo ; Shmaryahu, Amir ; Valdés, Jorge ; Dopson, Mark ; Rawlings, Douglas E. ; Banfield, Jillian F. ; Holmes, David S. ; Quatrini, Raquel. / Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus. En: PLoS ONE. 2013 ; Vol. 8, N.º 11.
@article{254cf669931946a8af36fda240263916,
title = "Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus",
abstract = "Background: Acidithiobacillus caldus is a sulfur oxidizing extreme acidophile and the only known mesothermophile within the Acidithiobacillales. As such, it is one of the preferred microbes for mineral bioprocessing at moderately high temperatures. In this study, we explore the genomic diversity of A. caldus strains using a combination of bioinformatic and experimental techniques, thus contributing first insights into the elucidation of the species pangenome. Principal Findings: Comparative sequence analysis of A. caldus ATCC 51756 and SM-1 indicate that, despite sharing a conserved and highly syntenic genomic core, both strains have unique gene complements encompassing nearly 20{\%} of their respective genomes. The differential gene complement of each strain is distributed between the chromosomal compartment, one megaplasmid and a variable number of smaller plasmids, and is directly associated to a diverse pool of mobile genetic elements (MGE). These include integrative conjugative and mobilizable elements, genomic islands and insertion sequences. Some of the accessory functions associated to these MGEs have been linked previously to the flexible gene pool in microorganisms inhabiting completely different econiches. Yet, others had not been unambiguously mapped to the flexible gene pool prior to this report and clearly reflect strain-specific adaption to local environmental conditions. Significance: For many years, and because of DNA instability at low pH and recurrent failure to genetically transform acidophilic bacteria, gene transfer in acidic environments was considered negligible. Findings presented herein imply that a more or less conserved pool of actively excising MGEs occurs in the A. caldus population and point to a greater frequency of gene exchange in this econiche than previously recognized. Also, the data suggest that these elements endow the species with capacities to withstand the diverse abiotic and biotic stresses of natural environments, in particular those associated with its extreme econiche.",
author = "Acu{\~n}a, {Lillian G.} and C{\'a}rdenas, {Juan Pablo} and Covarrubias, {Paulo C.} and Haristoy, {Juan Jos{\'e}} and Rodrigo Flores and Harold Nu{\~n}ez and Gonzalo Riadi and Amir Shmaryahu and Jorge Vald{\'e}s and Mark Dopson and Rawlings, {Douglas E.} and Banfield, {Jillian F.} and Holmes, {David S.} and Raquel Quatrini",
year = "2013",
month = "11",
day = "8",
doi = "10.1371/journal.pone.0078237",
language = "English",
volume = "8",
journal = "PLoS ONE",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "11",

}

Acuña, LG, Cárdenas, JP, Covarrubias, PC, Haristoy, JJ, Flores, R, Nuñez, H, Riadi, G, Shmaryahu, A, Valdés, J, Dopson, M, Rawlings, DE, Banfield, JF, Holmes, DS & Quatrini, R 2013, 'Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus', PLoS ONE, vol. 8, n.º 11, e78237. https://doi.org/10.1371/journal.pone.0078237

Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus. / Acuña, Lillian G.; Cárdenas, Juan Pablo; Covarrubias, Paulo C.; Haristoy, Juan José; Flores, Rodrigo; Nuñez, Harold; Riadi, Gonzalo; Shmaryahu, Amir; Valdés, Jorge; Dopson, Mark; Rawlings, Douglas E.; Banfield, Jillian F.; Holmes, David S.; Quatrini, Raquel.

En: PLoS ONE, Vol. 8, N.º 11, e78237, 08.11.2013.

Resultado de la investigación: Article

TY - JOUR

T1 - Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus

AU - Acuña, Lillian G.

AU - Cárdenas, Juan Pablo

AU - Covarrubias, Paulo C.

AU - Haristoy, Juan José

AU - Flores, Rodrigo

AU - Nuñez, Harold

AU - Riadi, Gonzalo

AU - Shmaryahu, Amir

AU - Valdés, Jorge

AU - Dopson, Mark

AU - Rawlings, Douglas E.

AU - Banfield, Jillian F.

AU - Holmes, David S.

AU - Quatrini, Raquel

PY - 2013/11/8

Y1 - 2013/11/8

N2 - Background: Acidithiobacillus caldus is a sulfur oxidizing extreme acidophile and the only known mesothermophile within the Acidithiobacillales. As such, it is one of the preferred microbes for mineral bioprocessing at moderately high temperatures. In this study, we explore the genomic diversity of A. caldus strains using a combination of bioinformatic and experimental techniques, thus contributing first insights into the elucidation of the species pangenome. Principal Findings: Comparative sequence analysis of A. caldus ATCC 51756 and SM-1 indicate that, despite sharing a conserved and highly syntenic genomic core, both strains have unique gene complements encompassing nearly 20% of their respective genomes. The differential gene complement of each strain is distributed between the chromosomal compartment, one megaplasmid and a variable number of smaller plasmids, and is directly associated to a diverse pool of mobile genetic elements (MGE). These include integrative conjugative and mobilizable elements, genomic islands and insertion sequences. Some of the accessory functions associated to these MGEs have been linked previously to the flexible gene pool in microorganisms inhabiting completely different econiches. Yet, others had not been unambiguously mapped to the flexible gene pool prior to this report and clearly reflect strain-specific adaption to local environmental conditions. Significance: For many years, and because of DNA instability at low pH and recurrent failure to genetically transform acidophilic bacteria, gene transfer in acidic environments was considered negligible. Findings presented herein imply that a more or less conserved pool of actively excising MGEs occurs in the A. caldus population and point to a greater frequency of gene exchange in this econiche than previously recognized. Also, the data suggest that these elements endow the species with capacities to withstand the diverse abiotic and biotic stresses of natural environments, in particular those associated with its extreme econiche.

AB - Background: Acidithiobacillus caldus is a sulfur oxidizing extreme acidophile and the only known mesothermophile within the Acidithiobacillales. As such, it is one of the preferred microbes for mineral bioprocessing at moderately high temperatures. In this study, we explore the genomic diversity of A. caldus strains using a combination of bioinformatic and experimental techniques, thus contributing first insights into the elucidation of the species pangenome. Principal Findings: Comparative sequence analysis of A. caldus ATCC 51756 and SM-1 indicate that, despite sharing a conserved and highly syntenic genomic core, both strains have unique gene complements encompassing nearly 20% of their respective genomes. The differential gene complement of each strain is distributed between the chromosomal compartment, one megaplasmid and a variable number of smaller plasmids, and is directly associated to a diverse pool of mobile genetic elements (MGE). These include integrative conjugative and mobilizable elements, genomic islands and insertion sequences. Some of the accessory functions associated to these MGEs have been linked previously to the flexible gene pool in microorganisms inhabiting completely different econiches. Yet, others had not been unambiguously mapped to the flexible gene pool prior to this report and clearly reflect strain-specific adaption to local environmental conditions. Significance: For many years, and because of DNA instability at low pH and recurrent failure to genetically transform acidophilic bacteria, gene transfer in acidic environments was considered negligible. Findings presented herein imply that a more or less conserved pool of actively excising MGEs occurs in the A. caldus population and point to a greater frequency of gene exchange in this econiche than previously recognized. Also, the data suggest that these elements endow the species with capacities to withstand the diverse abiotic and biotic stresses of natural environments, in particular those associated with its extreme econiche.

UR - http://www.scopus.com/inward/record.url?scp=84892656810&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0078237

DO - 10.1371/journal.pone.0078237

M3 - Article

C2 - 24250794

AN - SCOPUS:84892656810

VL - 8

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 11

M1 - e78237

ER -

Acuña LG, Cárdenas JP, Covarrubias PC, Haristoy JJ, Flores R, Nuñez H y otros. Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus. PLoS ONE. 2013 nov 8;8(11). e78237. https://doi.org/10.1371/journal.pone.0078237