Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments

Acid mine drainage (AMD), characterized by high concentrations of heavy metals and strong acidity, presents a significant challenge in environmental remediation. The acidophilic archaeon Ferroplasma facilitates soluble electron shuttles secreting and iron precipitate formation to immobilize heavy me...

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Main Authors: Yiran Li, Liyuan Ma, Shanshan Huang, Shiqi Chen, Shadab Begum, Nazidi Ibrahim, Yili Liang, Xueduan Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1654373/full
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author Yiran Li
Yiran Li
Liyuan Ma
Shanshan Huang
Shanshan Huang
Shiqi Chen
Shiqi Chen
Shadab Begum
Shadab Begum
Nazidi Ibrahim
Nazidi Ibrahim
Yili Liang
Yili Liang
Xueduan Liu
Xueduan Liu
author_facet Yiran Li
Yiran Li
Liyuan Ma
Shanshan Huang
Shanshan Huang
Shiqi Chen
Shiqi Chen
Shadab Begum
Shadab Begum
Nazidi Ibrahim
Nazidi Ibrahim
Yili Liang
Yili Liang
Xueduan Liu
Xueduan Liu
author_sort Yiran Li
collection DOAJ
description Acid mine drainage (AMD), characterized by high concentrations of heavy metals and strong acidity, presents a significant challenge in environmental remediation. The acidophilic archaeon Ferroplasma facilitates soluble electron shuttles secreting and iron precipitate formation to immobilize heavy metals and demonstrating significant remediation capabilities in microbial consortia. However, its environmental adaptation mechanisms in highly polluted environments during remediation remain unclear. Biosynthetic gene clusters (BGCs), which encode specialized metabolites with ecological roles, and mobile genetic elements (MGEs), known to mediate genomic function through gene disruption, rearrangement, and regulatory interference, represent crucial evolutionary means for environmental adaptation. In this study, Ferroplasma acidiphilum ZJ was screened from the traditional AMD of the Zijinshan copper mine, China. Then, it was sequenced, annotated and compared to three other sequenced Ferroplasma strains focusing on the distribution and function of genes concerning MGEs and BGCs. Genome-wide analysis indicated that MGEs, especially IS4 family insertion sequences (ISs) as well as genomic islands (GIs), were located close to functional regions, such as those related to heavy metal translocation, structural stability of cells, and the formation of archaeal ether-linked membranes. Further analysis showed Ferroplasma strains contained over 10 BGCs, with predicted functions spanning antibiotics, exopolysaccharide (EPS), and quorum sensing (QS). The Ferroplasma employed specialized MGEs and BGCs as key environmental adaptation mechanisms. This study provides a genetic framework for understanding the survival strategies of extremophiles in contaminated environments and explores the potential role of archaeal secondary metabolism (SM) in enhancing microbial processes for sustainable AMD bioremediation, by contributing to the detoxification and stabilization of heavy metals typically found in such environments.
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series Frontiers in Microbiology
spelling doaj-art-52c74930cd1c49d5ac9cfe8a3a0333f22025-08-20T03:31:38ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-07-011610.3389/fmicb.2025.16543731654373Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environmentsYiran Li0Yiran Li1Liyuan Ma2Shanshan Huang3Shanshan Huang4Shiqi Chen5Shiqi Chen6Shadab Begum7Shadab Begum8Nazidi Ibrahim9Nazidi Ibrahim10Yili Liang11Yili Liang12Xueduan Liu13Xueduan Liu14School of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaSchool of Environmental Studies, China University of Geosciences, Wuhan, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaSchool of Minerals Processing and Bioengineering, Central South University, Changsha, ChinaKey Laboratory of Biohydrometallurgy, Ministry of Education, Changsha, ChinaAcid mine drainage (AMD), characterized by high concentrations of heavy metals and strong acidity, presents a significant challenge in environmental remediation. The acidophilic archaeon Ferroplasma facilitates soluble electron shuttles secreting and iron precipitate formation to immobilize heavy metals and demonstrating significant remediation capabilities in microbial consortia. However, its environmental adaptation mechanisms in highly polluted environments during remediation remain unclear. Biosynthetic gene clusters (BGCs), which encode specialized metabolites with ecological roles, and mobile genetic elements (MGEs), known to mediate genomic function through gene disruption, rearrangement, and regulatory interference, represent crucial evolutionary means for environmental adaptation. In this study, Ferroplasma acidiphilum ZJ was screened from the traditional AMD of the Zijinshan copper mine, China. Then, it was sequenced, annotated and compared to three other sequenced Ferroplasma strains focusing on the distribution and function of genes concerning MGEs and BGCs. Genome-wide analysis indicated that MGEs, especially IS4 family insertion sequences (ISs) as well as genomic islands (GIs), were located close to functional regions, such as those related to heavy metal translocation, structural stability of cells, and the formation of archaeal ether-linked membranes. Further analysis showed Ferroplasma strains contained over 10 BGCs, with predicted functions spanning antibiotics, exopolysaccharide (EPS), and quorum sensing (QS). The Ferroplasma employed specialized MGEs and BGCs as key environmental adaptation mechanisms. This study provides a genetic framework for understanding the survival strategies of extremophiles in contaminated environments and explores the potential role of archaeal secondary metabolism (SM) in enhancing microbial processes for sustainable AMD bioremediation, by contributing to the detoxification and stabilization of heavy metals typically found in such environments.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1654373/fullenvironmental adaptationbioremediationsecondary metabolismmobile genetic elementFerroplasma
spellingShingle Yiran Li
Yiran Li
Liyuan Ma
Shanshan Huang
Shanshan Huang
Shiqi Chen
Shiqi Chen
Shadab Begum
Shadab Begum
Nazidi Ibrahim
Nazidi Ibrahim
Yili Liang
Yili Liang
Xueduan Liu
Xueduan Liu
Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments
Frontiers in Microbiology
environmental adaptation
bioremediation
secondary metabolism
mobile genetic element
Ferroplasma
title Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments
title_full Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments
title_fullStr Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments
title_full_unstemmed Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments
title_short Roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon Ferroplasma to extreme polluted environments
title_sort roles of mobile genetic elements and biosynthetic gene clusters in environmental adaptation of acidophilic archaeon ferroplasma to extreme polluted environments
topic environmental adaptation
bioremediation
secondary metabolism
mobile genetic element
Ferroplasma
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1654373/full
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