Comparative genomics reveals intraspecific divergence of Acidithiobacillus ferrooxidans: insights from evolutionary adaptation

Acidithiobacillus ferrooxidans serves as a model chemolithoautotrophic organism in extremely acidic environments, which has attracted much attention due to its unique metabolism and strong adaptability. However, little was known about the divergences along the evolutionary process based on whole genomes. Herein, we isolated six strains of A. ferrooxidans from mining areas in China and Zambia, and used comparative genomics to investigate the intra-species divergences. The results indicated that A. ferrooxidans diverged into three groups from a common ancestor, and the pan-genome is ‘open’. The ancestral reconstruction of A. ferrooxidans indicated that genome sizes experienced a trend of increase in the very earliest days before a decreasing tendency during the evolutionary process, suggesting that both gene gain and gene loss played crucial roles in A. ferrooxidans genome flexibility. Meanwhile, 23 single-copy orthologous groups (OGs) were under positive selection. The differences of rusticyanin (Rus) sequences (the key protein in the iron oxidation pathway) and type IV secretion system (T4SS) composition in the A. ferrooxidans were both related to their group divergences, which contributed to their intraspecific diversity. This study improved our understanding of the divergent evolution and environmental adaptation of A. ferrooxidans at the genome level in extreme conditions, which provided theoretical support for the survival mechanism of living creatures at the extreme.

[1]  M. Maiden,et al.  The Neisseria gonorrhoeae Accessory Genome and Its Association with the Core Genome and Antimicrobial Resistance , 2022, Microbiology spectrum.

[2]  Huiying Li,et al.  Integrative Assessments on Molecular Taxonomy of Acidiferrobacter thiooxydans ZJ and Its Environmental Adaptation Based on Mobile Genetic Elements , 2022, Frontiers in Microbiology.

[3]  D. Holmes,et al.  Integrative Genomics Sheds Light on Evolutionary Forces Shaping the Acidithiobacillia Class Acidophilic Lifestyle , 2022, Frontiers in Microbiology.

[4]  Liyuan Ma,et al.  Transcriptome analysis of an arsenite-/antimonite-oxidizer, Bosea sp. AS-1 reveals the importance of the type 4 secretion system in antimony resistance. , 2022, The Science of the total environment.

[5]  Farooq Sher,et al.  Microbial adaptation to different environmental conditions: molecular perspective of evolved genetic and cellular systems , 2022, Archives of Microbiology.

[6]  O. Massidda,et al.  FtsZ-Ring Regulation and Cell Division Are Mediated by Essential EzrA and Accessory Proteins ZapA and ZapJ in Streptococcus pneumoniae , 2021, Frontiers in Microbiology.

[7]  Hehuan Liao,et al.  The interaction of acidophiles driving community functional responses to the re-inoculated chalcopyrite bioleaching process. , 2021, The Science of the total environment.

[8]  D. Stokes,et al.  Structural basis for potassium transport in prokaryotes by KdpFABC , 2021, Proceedings of the National Academy of Sciences.

[9]  Qian Li,et al.  Comparative Genomics Provides Insights into the Genetic Diversity and Evolution of the DPANN Superphylum , 2021, mSystems.

[10]  K. Campbell,et al.  Genomic adaptations enabling Acidithiobacillus distribution across wide-ranging hot spring temperatures and pHs , 2021, Microbiome.

[11]  D. Johnson,et al.  Genomic evolution of the class Acidithiobacillia: deep-branching Proteobacteria living in extreme acidic conditions , 2021, The ISME Journal.

[12]  S. Lovett DNA polymerase III protein, HolC, helps resolve replication/transcription conflicts , 2021, Microbial cell.

[13]  Guanghong Zuo CVTree: A Parallel Alignment-free Phylogeny and Taxonomy Tool Based on Composition Vectors of Genomes , 2021, bioRxiv.

[14]  J. Xin,et al.  A Novel Lipoate-Protein Ligase, Mhp-LplJ, Is Required for Lipoic Acid Metabolism in Mycoplasma hyopneumoniae , 2021, Frontiers in Microbiology.

[15]  M. Li,et al.  Metagenomic insights into the metabolism and evolution of a new Thermoplasmata order (Candidatus Gimiplasmatales). , 2020, Environmental microbiology.

[16]  J. Kucera,et al.  A Model of Aerobic and Anaerobic Metabolism of Hydrogen in the Extremophile Acidithiobacillus ferrooxidans , 2020, Frontiers in Microbiology.

[17]  A. Kirschning The coenzyme/protein pair and the molecular evolution of life. , 2020, Natural product reports.

[18]  Delong Meng,et al.  Insights into the Metabolism and Evolution of the Genus Acidiphilium, a Typical Acidophile in Acid Mine Drainage , 2020, mSystems.

[19]  D. Downs,et al.  The Role of YggS in Vitamin B6 Homeostasis in Salmonella enterica Is Informed by Heterologous Expression of Yeast SNZ3 , 2020, Journal of Bacteriology.

[20]  S. Venter,et al.  Pan-Genome-Wide Analysis of Pantoea ananatis Identified Genes Linked to Pathogenicity in Onion , 2020, bioRxiv.

[21]  G. Southam,et al.  A widely distributed hydrogenase oxidises atmospheric H2 during bacterial growth , 2020, The ISME Journal.

[22]  P. Bork,et al.  Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity , 2020, The ISME Journal.

[23]  P. Stansfeld,et al.  Structural basis of proton-coupled potassium transport in the KUP family , 2020, Nature Communications.

[24]  M. Toll-Riera,et al.  Genetic dominance governs the evolution and spread of mobile genetic elements in bacteria , 2019, Proceedings of the National Academy of Sciences.

[25]  S. Kelly,et al.  OrthoFinder: phylogenetic orthology inference for comparative genomics , 2019, Genome Biology.

[26]  Xue-duan Liu,et al.  Phylogeny, Divergent Evolution, and Speciation of Sulfur-Oxidizing Acidithiobacillus Populations , 2019, BMC Genomics.

[27]  T. Fujishiro,et al.  Structure of sirohydrochlorin ferrochelatase SirB: the last of the structures of the class II chelatase family. , 2019, Dalton transactions.

[28]  B. Spira,et al.  Phosphate uptake by the phosphonate transport system PhnCDE , 2019, BMC Microbiology.

[29]  Wenjun Li,et al.  Insights into ecological role of a new deltaproteobacterial order Candidatus Acidulodesulfobacterales by metagenomics and metatranscriptomics , 2019, The ISME Journal.

[30]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v4: recent updates and new developments , 2019, Nucleic Acids Res..

[31]  Vincent J. Denef,et al.  Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions , 2019, mSphere.

[32]  Minliang Guo,et al.  Bacterial chemotaxis coupling protein: Structure, function and diversity. , 2019, Microbiological research.

[33]  C. Jin,et al.  1H, 13C and 15N resonance assignments of the second peptidyl-prolyl isomerase domain of chaperone SurA from Escherichia coli , 2019, Biomolecular NMR assignments.

[34]  Y. Li,et al.  Sulfur Oxidation in the Acidophilic Autotrophic Acidithiobacillus spp. , 2019, Front. Microbiol..

[35]  J. Tao,et al.  Comparative Genomic Analysis Reveals the Distribution, Organization, and Evolution of Metal Resistance Genes in the Genus Acidithiobacillus , 2018, Applied and Environmental Microbiology.

[36]  Xue-duan Liu,et al.  In Silico Genome-Wide Analysis Reveals the Potential Links Between Core Genome of Acidithiobacillus thiooxidans and Its Autotrophic Lifestyle , 2018, Front. Microbiol..

[37]  D. Johnson,et al.  Microbiomes in extremely acidic environments: functionalities and interactions that allow survival and growth of prokaryotes at low pH. , 2018, Current opinion in microbiology.

[38]  Y. Liu,et al.  Comparative transcriptome analysis of the invasive weed Mikania micrantha with its native congeners provides insights into genetic basis underlying successful invasion , 2018, BMC Genomics.

[39]  Xue-duan Liu,et al.  Pan-Genome Analysis Links the Hereditary Variation of Leptospirillum ferriphilum With Its Evolutionary Adaptation , 2018, Front. Microbiol..

[40]  Gabriel Waksman,et al.  Type IV secretion in Gram‐negative and Gram‐positive bacteria , 2018, Current Topics in Microbiology and Immunology.

[41]  S. Shima,et al.  Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction , 2017, Science.

[42]  M. Abanto,et al.  Physiological and comparative genomic analysis of Acidithiobacillus ferrivorans PQ33 provides psychrotolerant fitness evidence for oxidation at low temperature. , 2017, Research in microbiology.

[43]  Xue-duan Liu,et al.  Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss , 2017, Applied and Environmental Microbiology.

[44]  Xue-duan Liu,et al.  Gene Turnover Contributes to the Evolutionary Adaptation of Acidithiobacillus caldus: Insights from Comparative Genomics , 2016, Front. Microbiol..

[45]  N. Ravin,et al.  Effect of metal concentration on the microbial community in acid mine drainage of a polysulfide ore deposit , 2016, Microbiology.

[46]  Xue-duan Liu,et al.  Comparative genomics unravels metabolic differences at the species and/or strain level and extremely acidic environmental adaptation of ten bacteria belonging to the genus Acidithiobacillus. , 2016, Systematic and applied microbiology.

[47]  Xue-duan Liu,et al.  Metabolic diversity and adaptive mechanisms of iron- and/or sulfur-oxidizing autotrophic acidophiles in extremely acidic environments. , 2016, Environmental microbiology reports.

[48]  J. Tao,et al.  Comparative Genomics of the Extreme Acidophile Acidithiobacillus thiooxidans Reveals Intraspecific Divergence and Niche Adaptation , 2016, International journal of molecular sciences.

[49]  R. Daniel,et al.  Gene Loss and Horizontal Gene Transfer Contributed to the Genome Evolution of the Extreme Acidophile “Ferrovum” , 2016, Front. Microbiol..

[50]  Patricia P. Chan,et al.  tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes , 2016, Nucleic Acids Res..

[51]  C. Cañestro,et al.  Evolution by gene loss , 2016, Nature Reviews Genetics.

[52]  Chitra Dutta,et al.  BPGA- an ultra-fast pan-genome analysis pipeline , 2016, Scientific Reports.

[53]  Christopher L. Hemme,et al.  Lateral Gene Transfer in a Heavy Metal-Contaminated-Groundwater Microbial Community , 2016, mBio.

[54]  C. Navarro,et al.  Cytoplasmic CopZ-Like Protein and Periplasmic Rusticyanin and AcoP Proteins as Possible Copper Resistance Determinants in Acidithiobacillus ferrooxidans ATCC 23270 , 2015, Applied and Environmental Microbiology.

[55]  Jörg Peplies,et al.  JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison , 2015, Bioinform..

[56]  Connor T. Skennerton,et al.  CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes , 2015, Genome research.

[57]  M. Ferrer,et al.  Microbial diversity and metabolic networks in acid mine drainage habitats , 2015, Front. Microbiol..

[58]  David R. Riley,et al.  Ten years of pan-genome analyses. , 2015, Current opinion in microbiology.

[59]  W. Shu,et al.  Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage , 2014, The ISME Journal.

[60]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[61]  Xiang-mei Liu,et al.  A versatile and efficient markerless gene disruption system for Acidithiobacillus thiooxidans: application for characterizing a copper tolerance related multicopper oxidase gene. , 2014, Environmental microbiology.

[62]  S. Giovannoni,et al.  Implications of streamlining theory for microbial ecology , 2014, The ISME Journal.

[63]  Andreas Wagner,et al.  Growth Temperature and Genome Size in Bacteria Are Negatively Correlated, Suggesting Genomic Streamlining During Thermal Adaptation , 2013, Genome biology and evolution.

[64]  David W. Cheung,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.

[65]  Damian Szklarczyk,et al.  STRING v9.1: protein-protein interaction networks, with increased coverage and integration , 2012, Nucleic Acids Res..

[66]  Young Cheol Kim,et al.  Comparative Genomics of Plant-Associated Pseudomonas spp.: Insights into Diversity and Inheritance of Traits Involved in Multitrophic Interactions , 2012, PLoS genetics.

[67]  C. Arraiano,et al.  Characterization of the BolA homolog IbaG: a new gene involved in acid resistance. , 2012, Journal of microbiology and biotechnology.

[68]  Haiyan Zhang,et al.  ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. , 2012, Biochemical and biophysical research communications.

[69]  R. Lenski,et al.  The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss , 2012, mBio.

[70]  Judith P. Armitage,et al.  Signal processing in complex chemotaxis pathways , 2011, Nature Reviews Microbiology.

[71]  C. Häse,et al.  Insights into the biochemistry of the ubiquitous NhaP family of cation/H+ antiporters. , 2011, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[72]  Hongwei Wu,et al.  Gene-centric association analysis for the correlation between the guanine-cytosine content levels and temperature range conditions of prokaryotic species , 2010, BMC Bioinformatics.

[73]  Miklós Csuös,et al.  Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood , 2010, Bioinform..

[74]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[75]  R. Rosselló-Móra,et al.  Shifting the genomic gold standard for the prokaryotic species definition , 2009, Proceedings of the National Academy of Sciences.

[76]  Geoffrey J. Barton,et al.  Jalview Version 2—a multiple sequence alignment editor and analysis workbench , 2009, Bioinform..

[77]  Inti Pedroso,et al.  Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: Insights into their metabolism and ecophysiology , 2008 .

[78]  David R. Riley,et al.  Comparative genomics: the bacterial pan-genome. , 2008, Current opinion in microbiology.

[79]  Cindy J. Castelle,et al.  A New Iron-oxidizing/O2-reducing Supercomplex Spanning Both Inner and Outer Membranes, Isolated from the Extreme Acidophile Acidithiobacillus ferrooxidans* , 2008, Journal of Biological Chemistry.

[80]  Haïtham Sghaier,et al.  Basal DNA repair machinery is subject to positive selection in ionizing-radiation-resistant bacteria , 2008, BMC Genomics.

[81]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[82]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[83]  G. Qiu,et al.  Research on isc Operon in Acidithiobacillus ferrooxidans ATCC 23270 , 2007 .

[84]  Peter F. Hallin,et al.  RNAmmer: consistent and rapid annotation of ribosomal RNA genes , 2007, Nucleic acids research.

[85]  C. Baker-Austin,et al.  Life in acid: pH homeostasis in acidophiles. , 2007, Trends in microbiology.

[86]  G. Cook,et al.  The Phn system of Mycobacterium smegmatis: a second high-affinity ABC-transporter for phosphate. , 2006, Microbiology.

[87]  R. Nielsen Molecular signatures of natural selection. , 2005, Annual review of genetics.

[88]  L. Alcaraz,et al.  Unfolding process of rusticyanin: evidence of protein aggregation. , 2004, European journal of biochemistry.

[89]  H. Kazazian Mobile Elements: Drivers of Genome Evolution , 2004, Science.

[90]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[91]  E. Cascales,et al.  The versatile bacterial type IV secretion systems , 2003, Nature Reviews Microbiology.

[92]  G. Southam,et al.  A critical stage in the formation of acid mine drainage: Colonization of pyrite by Acidithiobacillus ferrooxidans under pH‐neutral conditions , 2003 .

[93]  Frederico J. Gueiros-Filho,et al.  A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. , 2002, Genes & development.

[94]  R. Hedderich,et al.  Heterodisulfide reductase from Methanothermobacter marburgensis contains an active‐site [4Fe–4S] cluster that is directly involved in mediating heterodisulfide reduction , 2002, FEBS letters.

[95]  Hachiro Inokuchi,et al.  HemK, a class of protein methyl transferase with similarity to DNA methyl transferases, methylates polypeptide chain release factors, and hemK knockout induces defects in translational termination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[96]  B. Barrell,et al.  Massive gene decay in the leprosy bacillus , 2001, Nature.

[97]  Violaine Bonnefoy,et al.  Characterization of an Operon Encoding Two c-Type Cytochromes, an aa3-Type Cytochrome Oxidase, and Rusticyanin in Thiobacillus ferrooxidansATCC 33020 , 1999, Applied and Environmental Microbiology.

[98]  M. Kimura Evolutionary Rate at the Molecular Level , 1968, Nature.

[99]  K. Temple,et al.  THE AUTOTROPHIC OXIDATION OF IRON BY A NEW BACTERIUM: THIOBACILLUS FERROOXIDANS , 1951, Journal of bacteriology.

[100]  T. Shimada,et al.  Identification of YbhA as the pyridoxal 5'-phosphate (PLP) phosphatase in Escherichia coli: Importance of PLP homeostasis on the bacterial growth. , 2018, The Journal of general and applied microbiology.

[101]  S. Backert,et al.  Erratum to: Type IV Secretion in Gram-Negative and Gram-Positive Bacteria. , 2017, Current topics in microbiology and immunology.

[102]  Daniel C. Jeffares,et al.  A beginners guide to estimating the non-synonymous to synonymous rate ratio of all protein-coding genes in a genome. , 2015, Methods in molecular biology.

[103]  C. Brochier-Armanet,et al.  Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. , 2011, Microbiology.

[104]  Susumu Goto,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[105]  M V Olson,et al.  When less is more: gene loss as an engine of evolutionary change. , 1999, American journal of human genetics.

[106]  H. S. Heaps,et al.  Information retrieval, computational and theoretical aspects , 1978 .