Genomic evolution of the class Acidithiobacillia: deep-branching Proteobacteria living in extreme acidic conditions

Abstract

Members of the genus Acidithiobacillus, now ranked within the class Acidithiobacillia, are model bacteria for the study of chemolithotrophic energy conversion under extreme conditions. Knowledge of the genomic and taxonomic diversity of Acidithiobacillia is still limited. Here, we present a systematic analysis of nearly 100 genomes from the class sampled from a wide range of habitats. Some of these genomes are new and others have been reclassified on the basis of advanced genomic analysis, thus defining 19 Acidithiobacillia lineages ranking at different taxonomic levels. This work provides the most comprehensive classification and pangenomic analysis of this deep-branching class of Proteobacteria to date. The phylogenomic framework obtained illuminates not only the evolutionary past of this lineage, but also the molecular evolution of relevant aerobic respiratory proteins, namely the cytochrome bo3 ubiquinol oxidases.

Integrative Genomics Sheds Light on Evolutionary Forces Shaping the Acidithiobacillia Class Acidophilic Lifestyle

“…The acidophiles were further grouped into nine clades, of which two represented different genera (clades 2 and 3); meanwhile, clades 4–10 grouped species from the Acidithiobacillus genus, which is divided into clades according to their capacity to obtain energy such as sulfur oxidizers (clades 4 and 5) and iron/sulfur oxidizers (clades 6–10). While the association between the Acidithiobacillaceae and Thermithiobacillaceae families was consistent with previous analyses ( Williams et al, 2010 ; Williams and Kelly, 2013 ; Boden et al, 2016 ; Moya-Beltrán et al, 2021 ), the tree also suggested a need for deeper phylogenomic analysis such as for the Acidithiobacillus clade, questioning if this clade includes more than a single genus according to their energy properties. Representative genomes from the ten clades of the core tree were selected for this study with their accession numbers and isolation data summarized in Table 1 .…”

“…Due to their acidophilic nature, the Acidithiobacillaceae are largely recalcitrant to standard genetic manipulation ( Inaba et al, 2018 ; Jung et al, 2021 ), and consequently, the use of bioinformatics approaches advances our understanding of the biology of these extremophiles. The research of Moya-Beltrán et al (2021) describes four Acidithiobacillaceae genera ( Nuñez et al, 2016 ), namely, (i) sulfur oxidizing Ambacidithiobacillus that includes the recently described species Am. sulfuriphilus (ex Acidithiobacillus sulfuriphilus ) ( Falagán et al, 2019 ); (ii) Igneacidithiobacillus including species I. copahuensis ( Moya-Beltrán et al, 2021 ), Candidatus I. taiwanensis ( Moya-Beltrán et al, 2021 ), and Candidatus I. yellowstonensis ( Moya-Beltrán et al, 2021 ); (iii) Fervidacidithiobacillus with F. caldus (ex- Acidithiobacillus caldus ) ( Hallberg and Lindström, 1994 ; Valdes et al, 2009 ; You et al, 2011 ; Zhang et al, 2016b ); and (iv) the Acidithiobacillus genus formed by A. thiooxidans ( Waksman and Joffe, 1922 ; Valdes et al, 2011 ; Travisany et al, 2014 ; Yin et al, 2014 ; Zhang et al, 2016a , 2018 ; Quatrini et al, 2017 ; Camacho et al, 2020 ), A. albertensis ( Bryant et al, 1983 ; Castro et al, 2017 ), Acidithiobacillus sp.…”

“…The research of Moya-Beltrán et al (2021) describes four Acidithiobacillaceae genera ( Nuñez et al, 2016 ), namely, (i) sulfur oxidizing Ambacidithiobacillus that includes the recently described species Am. sulfuriphilus (ex Acidithiobacillus sulfuriphilus ) ( Falagán et al, 2019 ); (ii) Igneacidithiobacillus including species I. copahuensis ( Moya-Beltrán et al, 2021 ), Candidatus I. taiwanensis ( Moya-Beltrán et al, 2021 ), and Candidatus I. yellowstonensis ( Moya-Beltrán et al, 2021 ); (iii) Fervidacidithiobacillus with F. caldus (ex- Acidithiobacillus caldus ) ( Hallberg and Lindström, 1994 ; Valdes et al, 2009 ; You et al, 2011 ; Zhang et al, 2016b ); and (iv) the Acidithiobacillus genus formed by A. thiooxidans ( Waksman and Joffe, 1922 ; Valdes et al, 2011 ; Travisany et al, 2014 ; Yin et al, 2014 ; Zhang et al, 2016a , 2018 ; Quatrini et al, 2017 ; Camacho et al, 2020 ), A. albertensis ( Bryant et al, 1983 ; Castro et al, 2017 ), Acidithiobacillus sp. SH ( Kamimura et al, 2018 ) plus the iron/sulfur oxidizers A. ferrooxidans ( Temple and Colmer, 1951 ; Valdés et al, 2008 ; Chen P. et al, 2015 ; Yan et al, 2015 ; Kucera et al, 2016 ; Ulloa et al, 2019 ), A. ferridurans ( Hedrich and Johnson, 2013 ; Miyauchi et al, 2018 ), A. ferrivorans ( Hallberg et al, 2010 ; Liljeqvist et al, 2011 ; Talla et al, 2014 ; Tran et al, 2017 ), and A. ferriphilus ( Falagán and Johnson, 2016 ) represented by A. ferrooxidans BY0502 for which phylogenetic and nucleotide identity analysis is suggested to be reclassified as an A. ferriphilus -like species ( González et al, 2016 ; Fariq et al, 2019 ).…”

Chromium (VI) Inhibition of Low pH Bioleaching of Limonitic Nickel-Cobalt Ore

“…sulfidivorans T , and At. caldus strain BRGM3 ( Moya-Beltrán et al, 2021 ). Cultures were sourced from the Acidophile Culture Collection maintained at Bangor University except for the Acidianus species which were obtained from the German Collection of Microorganisms and Cell Cultures (DSMZ, Germany).…”

Recent progress in the application of omics technologies in the study of bio-mining microorganisms from extreme environments

“…A. ferrooxidans YNTRS-40, ATCC 23270, ATCC 53993 YQH-1 [9] CCM 4253, DSM 16786 [10], Hel18, PQ506 [10], PQ505 [10], CF3 [10], F221, BY0502, RVS1, DLC-5 [11], COP1 [10], S10 [10], BY-3 [12], ATCC 8085 [10], ZBY, DMC [12], A02 [12], Licanantay [13], JYC-17 [12], ATCC 15494 [10], BY-02 [12], A01 [14] A. caldus MTH-04, ATCC 51756 [15], SM-1 [16] KU [10], CV18-1 [10], 6 [10], MELC5 [10], BC13 [10], VAN18-3 [10], DX [17], ZBY [17], ZJ [17], MNG [10], C-SH12 [10], F [10], S1 [17] L. ferrooxidans C2-3 [18] L. ferriphilum ML-04 [19], YSK [20] UBA6657 [21], UBA5695 [21], UBA6673 [21], UBA6674 [21], UBA7872 [21], UBA7391 [21], UBA7384 [21], UBA7870 [21], UBA7392 [21], UBA6677 [21] DSM 14647 [22], pb_238, DX…”