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Genome-Based Classification of Two TAXONOMIC DESCRIPTION Khaleque et al., Int J Syst Evol Microbiol DOI 10.1099/ijsem.0.003313 Genome-based classification of two halotolerant extreme acidophiles, Acidihalobacter prosperus V6 (=DSM 14174 =JCM 32253) and ’Acidihalobacter ferrooxidans’ V8 (=DSM 14175 =JCM 32254) as two new species, Acidihalobacter aeolianus sp. nov. and Acidihalobacter ferrooxydans sp. nov., respectively Himel N. Khaleque,1,2† Carolina Gonzalez, 3† Anna H. Kaksonen,2 Naomi J. Boxall,2 David S. Holmes3,* and Elizabeth L. J. Watkin1,* Abstract Phylogenomic analysis of recently released high-quality draft genome sequences of the halotolerant acidophiles, Acidihalobacter prosperus V6 (=DSM 14174=JCM 32253) and ‘Acidihalobacter ferrooxidans’ V8 (=DSM 14175=JCM 32254), was undertaken in order to clarify their taxonomic relationship. Sequence based phylogenomic approaches included 16S rRNA gene phylogeny, multi-gene phylogeny from the concatenated alignment of nine selected housekeeping genes and multiprotein phylogeny using clusters of orthologous groups of proteins from ribosomal protein families as well as those from complete sets of markers based on concatenated alignments of universal protein families. Non-sequence based approaches for species circumscription were based on analyses of average nucleotide identity, which was further reinforced by the correlation indices of tetra-nucleotide signatures as well as genome-to-genome distance (digital DNA–DNA hybridization) calculations. The different approaches undertaken in this study for species tree reconstruction resulted in a tree that was phylogenetically congruent, revealing that both micro-organisms are members of separate species of the genus Acidihalobacter. In accordance, it is proposed that A. prosperus V6T (=DSM 14174 T=JCM 32253 T) be formally classified as Acidihalobacter aeolianus sp. nov., and ‘Acidihalobacter ferrooxidans’ V8T (=DSM 14175 T=JCM 32254 T) as Acidihalobacter ferrooxydans sp. nov., and that both represent the type strains of their respective species. Only a few bacteria capable of simultaneously tolerating The genus Acidihalobacter includes only one formally recog- both low pH and high salt have been isolated [1, 2]. There- nized species name, Acidihalobacter prosperus [4]. A. pros- fore, the discovery and characterization of new species of perus DSM 5130T is an iron- and sulfur-oxidizing, halotolerant acidophiles enriches the opportunities to map mesophilic, halotolerant acidophile that was isolated from a the microbial diversity and shed new light on the metabolic geothermally heated seafloor at Porto di Levante, Vulcano, capabilities in this mostly unexplored geochemical environ- Italy [5]. Based on its phenotype and a G+C content of ment. It could also suggest novel routes by which the meta- 64 mol%, it was originally taxonomically classified as bolic potential of halotolerant acidophiles could be ‘ ’ exploited for industrial applications such as copper biol- Thiobacillus prosperus by Huber and Stetter [5]. However, eaching from chalcopyrite [3]. This is an especially import- after the release of its draft genome sequence [6], further phy- ant consideration in regions with scarce water resources logenomic studies were undertaken and it was formally such as Australia and Chile where sea water could be substi- reclassified into the family Ectothiorhodospiraceae of the class tuted for fresh water in the bioleaching process [2]. Gammaproteobacteria in the new genus Acidihalobacter, Author affiliations: 1School of Pharmacy and Biomedical Sciences, Curtin Health Innovation Research Institute, Curtin University, Perth, Australia; 2CSIRO Land and Water, Floreat, Australia; 3Center for Bioinformatics and Genome Biology, Fundacion Ciencia y Vida and Facultad de Ciencias Biologicas, Universidad Andres Bello, Santiago, Chile. *Correspondence: David S. Holmes, [email protected]; Elizabeth L. J. Watkin, [email protected] Keywords: Acidophile; iron and sulfur oxidising; halotolerant. Abbreviations: AIC, Akaike information criteria; ANI, average nucleotide identity; ANIb, average nucleotide identity based on BLAST; BIC, Bayesian information criteria; COGs, clusters of orthologous groups of proteins; dDDH, digital DNA–DNA hybridization; MLSA, multilocus sequence analysis; NIB, nucleotide identity by BLAST; Tetra, tetra-nucleotide signatures. †These authors contributed equally to this work. Acidihalobacter prosperus V6: chromosome, CP017448.1; plasmid, CP017449.1. ‘Acidihalobacter ferrooxidans’ V8: CP019434.1. Four supplementary tables are available with the online version of this article. 003313 ã 2019 The Authors Downloaded from www.microbiologyresearch.org by This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. IP: 190.153.178.170 1 On: Thu, 11 Apr 2019 18:47:41 Khaleque et al., Int J Syst Evol Microbiol with A. prosperus DSM 5130T (JCM 30709T) being named [15, 16]. Whole-genome sequencing has shown the pres- the type strain of its species [4]. ence of a 162 484 bp plasmid in A. prosperus V6 that is not present in either the type strain of A. prosperus or in More recently, two new halotolerant acidophiles, A. pros- ‘A. ferrooxidans’ V8 [6, 15, 16]. We term this plasmid perus V6 and ‘A. ferrooxidans’ V8, were isolated from mixed pABPV6. The availability of the high quality draft environmental cultures obtained from shallow acidic pools genomes of these strains has provided an opportunity to on the Aeolian Islands, Vulcano, Italy [7]. A. prosperus V6 use phylogenomic strategies for the re-evaluation of the was recognized to be similar to the type strain in its 16S taxonomical positions of both species in order to properly rRNA gene phylogeny as well as its morphological charac- classify them [17]. Predicted terminal oxidases from the teristics [8, 9], but showed superior growth to the type strain genomes of A. prosperus V6 and ‘A. ferrooxidans’ V8 on ferrous iron [5, 10]. A. prosperus V6 was shown to be a include aa (EC 1.9.3.1), bo (EC 1.10.3.10), bd-I (EC member of the family Ectothiorhodospiraceae of the class 3 3 1.10.3.14) and fumarate reductase (quinol, EC 1.3.5.1– Gammaproteobacteria [11]. It has previously been referred 1.3.5.4). Predicted respiratory quinones from the genomes to as ‘Acidihalobacter aeolicus’ [12]; however, based on 99 % include ubiquinone (EC 1.14.13.-, 2.1.1.64, 2.1.1.63, 16S rRNA gene sequence similarity as well as similarity in T 2.1.1.201, 2.1.1.222, 2.5.1.39, 2.5.1.129, 4.1.1.98). its morphological characteristics to A. prosperus DSM 5130 (‘Thiobacillus prosperus’ at the time), it was submitted to the Recent proteomic studies have found ectoine to be the DSMZ culture collection as a strain of the A. prosperus spe- major osmoprotectant in A. prosperus DSM 5130T [18] and cies and was never formally classified or named. A. prosperus V6 [19] and it is presumed it will also play a key role in osmoprotection of ‘A. ferrooxidans’ V8, as pre- A. prosperus V6 is an aerobe, grows autotrophically and is able to oxidize ferrous iron, the sulfur sources elemental sul- liminary analysis of the genomes of all three isolates has fur and tetrathionate and the sulfide mineral pyrite. It is shown the presence of genes for the synthesis of ectoine unable to grow in the absence of chloride, requiring a mini- [6, 15, 16]. However, differences in the genomes of the three mum of 60 mM NaCl, is able to grow at up to 1283 mM NaCl isolates included the presence of a truncated SOX operon (soxAXBYZ) in A. prosperus DSM 5130 T and A. prosperus with maximum growth at 428 mM NaCl [8, 13]. It is able to ‘ ’ oxidize pyrite at an optimum 256 mM NaCl [13]. The tem- V6 that was not found on the genome of A. ferrooxidans perature range for growth of A. prosperus V6 was 26–42 C V8 [6, 15, 16]. with an optimum of 36 C [14]. Growth at various pH values The bioinformatically inferred G+C contents for the À1 was determined in basal salts medium [2] at 25 g l NaCl genomes of A. prosperus V6 and ‘A. ferrooxidans’ V8 are Á with 50 mM FeSO4 7H2O and 5 mM K2S4O6 [13]. A. pros- 62.2 and 61.6 mol%, respectively [15]. These values fall perus V6 was able to grow between pH 1.5 and 3.0, but not at within the range of 50.5–69.7 mol% DNA G+C for members pH 1.0 and 3.5 with optimum growth observed at pH 1.8. of the family Ectothiorhodospiraceae [20]. It is also consis- Similarly, ‘A. ferrooxidans’ V8 was submitted to the DSMZ tent with the placement of the two species in the genus culture collection with its current name as it was was Acidihalobacter, which is nearest to the Ectothiorhodospira thought to belong to a new species of the genus Acidihalo- genus, both of which show a requirement of chloride for bacter based on its 16S rRNA gene sequence and pheno- growth [4, 5, 8, 20]. Phenotypic and genomic features of the typic characteristics such as slightly greater chloride ion three species of the genus Acidihalobacter are shown in tolerance than A. prosperus V6 when grown on the sulfide Table 1. mineral pyrite [9, 10]. However, it was never characterized In order to infer preliminary phylogenetic relationships, the taxonomically in detail. It is aerobic and autotrophic, able 16S rRNA gene sequence similarity of A. prosperus V6, ‘A. to oxidize ferrous iron, elemental sulfur and tetrathionate ferrooxidans’ V8 and A. prosperus DSM 5130T was com- and the sulfide mineral pyrite, and is unable to grow in the pared by aligning the sequences using the default settings of absence of chloride, having a minimum requirement of the nucleotide Basic Local Alignment Search Tool (BLASTn) more than 60 mM NaCl when grown in the presence of tool [21] and MAFFT alignment (using the L-INS-i iterative soluble iron [13]. Maximum growth on ferrous iron and refinement) [22, 23].
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