Influence of mobile genetic elements and insertion sequences in long- and short-term adaptive processes of Acidithiobacillus ferrooxidans strains

Ana Moya-Beltrán, Martin Gajdosik, Camila Rojas-Villalobos, Simón Beard, Martin Mandl, Danitza Silva-García, D. Barrie Johnson, Pablo Ramirez, Raquel Quatrini, Jiri Kucera

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)
9 Downloads (Pure)

Abstract

The recent revision of the Acidithiobacillia class using genomic taxonomy methods has shown that, in addition to the existence of previously unrecognized genera and species, some species of the class harbor levels of divergence that are congruent with ongoing differentiation processes. In this study, we have performed a subspecies-level analysis of sequenced strains of Acidithiobacillus ferrooxidans to prove the existence of distinct sublineages and identify the discriminant genomic/genetic characteristics linked to these sublineages, and to shed light on the processes driving such differentiation. Differences in the genomic relatedness metrics, levels of synteny, gene content, and both integrated and episomal mobile genetic elements (MGE) repertoires support the existence of two subspecies-level taxa within A. ferrooxidans. While sublineage 2A harbors a small plasmid related to pTF5, this episomal MGE is absent in sublineage 2B strains. Likewise, clear differences in the occurrence, coverage and conservation of integrated MGEs are apparent between sublineages. Differential MGE-associated gene cargo pertained to the functional categories of energy metabolism, ion transport, cell surface modification, and defense mechanisms. Inferred functional differences have the potential to impact long-term adaptive processes and may underpin the basis of the subspecies-level differentiation uncovered within A. ferrooxidans. Genome resequencing of iron- and sulfur-adapted cultures of a selected 2A sublineage strain (CCM 4253) showed that both episomal and large integrated MGEs are conserved over twenty generations in either growth condition. In turn, active insertion sequences profoundly impact short-term adaptive processes. The ISAfe1 element was found to be highly active in sublineage 2A strain CCM 4253. Phenotypic mutations caused by the transposition of ISAfe1 into the pstC2 encoding phosphate-transport system permease protein were detected in sulfur-adapted cultures and shown to impair growth on ferrous iron upon the switch of electron donor. The phenotypic manifestation of the △pstC2 mutation, such as a loss of the ability to oxidize ferrous iron, is likely related to the inability of the mutant to secure the phosphorous availability for electron transport-linked phosphorylation coupled to iron oxidation. Depletion of the transpositional △pstC2 mutation occurred concomitantly with a shortening of the iron-oxidation lag phase at later transfers on a ferrous iron-containing medium. Therefore, the pstII operon appears to play an essential role in A. ferrooxidans when cells oxidize ferrous iron. Results highlight the influence of insertion sequences and both integrated and episomal mobile genetic elements in the short- and long-term adaptive processes of A. ferrooxidans strains under changing growth conditions.
Original languageEnglish
Article number10876
Number of pages16
JournalScientific Reports
Volume13
Issue number1
Early online date5 Jul 2023
DOIs
Publication statusE-pub ahead of print - 5 Jul 2023

Bibliographical note

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder

Funder

This work was funded by a subsidy for the development of the research institution and by the Masaryk University Program, project no. MUNI/A/1313/2022 (M.G., J.K., M.M.). This work was supported by the Agencia Nacional de Investigación y Desarrollo (ANID) under Grants FONDECYT 1221035 (R.Q.), Centro Ciencia & Vida, FB210008, Financiamiento Basal para Centros Científicos y Tecnológicos de Excelencia (R.Q.), Vicerrectoría de Investigación y Doctorados de la Universidad San Sebastián, Project USS-FIN-23-PDOC-03 (A.M-B.) and PhD scholarship (C.R-V.), and by Fundación Ciencia and Vida Hinge PostDoc Program (S.B.). Funding Information: This work was funded by a subsidy for the development of the research institution and by the Masaryk University Program, project no. MUNI/A/1313/2022 (M.G., J.K., M.M.). This work was supported by the Agencia Nacional de Investigación y Desarrollo (ANID) under Grants FONDECYT 1221035 (R.Q.), Centro Ciencia & Vida, FB210008, Financiamiento Basal para Centros Científicos y Tecnológicos de Excelencia (R.Q.), Vicerrectoría de Investigación y Doctorados de la Universidad San Sebastián, Project USS-FIN-23-PDOC-03 (A.M-B.) and PhD scholarship (C.R-V.), and by Fundación Ciencia and Vida Hinge PostDoc Program (S.B.). Publisher Copyright: © 2023, The Author(s).

Keywords

  • Acidithiobacillus - genetics - metabolism
  • DNA Transposable Elements - genetics
  • Iron - metabolism
  • Oxidation-Reduction
  • Sulfur - metabolism

Fingerprint

Dive into the research topics of 'Influence of mobile genetic elements and insertion sequences in long- and short-term adaptive processes of Acidithiobacillus ferrooxidans strains'. Together they form a unique fingerprint.

Cite this