Novel adaptive immune systems in pristine Antarctic soils

Abstract Antarctic environments are dominated by microorganisms, which are vulnerable to viral infection. Although several studies have investigated the phylogenetic repertoire of bacteria and viruses in these poly-extreme environments with freezing temperatures, high ultra violet irradiation levels...

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Main Authors: Marc W. Van Goethem, Oliver K. I. Bezuidt, Rian Pierneef, Surendra Vikram, David W. Hopkins, Thomas Aspray, Grant Hall, Stephan Woodborne, Ian D. Hogg, Trent R. Northen, Weidong Kong, Daniele Daffonchio, Don A. Cowan, Yves Van de Peer, Manuel Delgado-Baquerizo, Thulani P. Makhalanyane
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-83942-y
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author Marc W. Van Goethem
Oliver K. I. Bezuidt
Rian Pierneef
Surendra Vikram
David W. Hopkins
Thomas Aspray
Grant Hall
Stephan Woodborne
Ian D. Hogg
Trent R. Northen
Weidong Kong
Daniele Daffonchio
Don A. Cowan
Yves Van de Peer
Manuel Delgado-Baquerizo
Thulani P. Makhalanyane
author_facet Marc W. Van Goethem
Oliver K. I. Bezuidt
Rian Pierneef
Surendra Vikram
David W. Hopkins
Thomas Aspray
Grant Hall
Stephan Woodborne
Ian D. Hogg
Trent R. Northen
Weidong Kong
Daniele Daffonchio
Don A. Cowan
Yves Van de Peer
Manuel Delgado-Baquerizo
Thulani P. Makhalanyane
author_sort Marc W. Van Goethem
collection DOAJ
description Abstract Antarctic environments are dominated by microorganisms, which are vulnerable to viral infection. Although several studies have investigated the phylogenetic repertoire of bacteria and viruses in these poly-extreme environments with freezing temperatures, high ultra violet irradiation levels, low moisture availability and hyper-oligotrophy, the evolutionary mechanisms governing microbial immunity remain poorly understood. Using genome-resolved metagenomics, we test the hypothesis that Antarctic poly-extreme high-latitude microbiomes harbour diverse adaptive immune systems. Our analysis reveals the prevalence of prophages in bacterial genomes (Bacteroidota and Verrucomicrobiota), suggesting the significance of lysogenic infection strategies in Antarctic soils. Furthermore, we demonstrate the presence of diverse CRISPR-Cas arrays, including Class 1 arrays (Types I-B, I-C, and I-E), alongside systems exhibiting novel gene architecture among their effector cas genes. Notably, a Class 2 system featuring type V variants lacks CRISPR arrays, encodes Cas1 and Cas2 adaptation module genes. Phylogenetic analysis of Cas12 effector proteins hints at divergent evolutionary histories compared to classified type V effectors and indicates that TnpB is likely the ancestor of Cas12 nucleases. Our findings suggest substantial novelty in Antarctic cas sequences, likely driven by strong selective pressures. These results underscore the role of viral infection as a key evolutionary driver shaping polar microbiomes.
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spelling doaj-art-44742c98bdf846c58a2c46774e78d02f2025-01-19T12:23:57ZengNature PortfolioScientific Reports2045-23222025-01-0115111410.1038/s41598-024-83942-yNovel adaptive immune systems in pristine Antarctic soilsMarc W. Van Goethem0Oliver K. I. Bezuidt1Rian Pierneef2Surendra Vikram3David W. Hopkins4Thomas Aspray5Grant Hall6Stephan Woodborne7Ian D. Hogg8Trent R. Northen9Weidong Kong10Daniele Daffonchio11Don A. Cowan12Yves Van de Peer13Manuel Delgado-Baquerizo14Thulani P. Makhalanyane15Department of Biochemistry, Genetics and Microbiology, University of PretoriaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, University of PretoriaDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, University of PretoriaDepartment of Biochemistry, Genetics and Microbiology, University of PretoriaScotland’s Rural CollegeSchool of Energy, Geoscience, Infrastructure and Society, Heriot-Watt UniversityMammal Research Institute, University of PretoriaiThemba LABSCanadian High Arctic Research Station, Polar Knowledge Canada; and School of Science, University of WaikatoMolecular EcoSystems Biology Division, Lawrence Berkeley National LaboratoryState Key Laboratory of Tibetan Plateau Earth System and Resources Environment, Institute of Tibetan Plateau Research, Chinese Academy of SciencesBiological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and TechnologyDepartment of Biochemistry, Genetics and Microbiology, University of PretoriaDepartment of Biochemistry, Genetics and Microbiology, University of PretoriaLaboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSICDepartment of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, University of PretoriaAbstract Antarctic environments are dominated by microorganisms, which are vulnerable to viral infection. Although several studies have investigated the phylogenetic repertoire of bacteria and viruses in these poly-extreme environments with freezing temperatures, high ultra violet irradiation levels, low moisture availability and hyper-oligotrophy, the evolutionary mechanisms governing microbial immunity remain poorly understood. Using genome-resolved metagenomics, we test the hypothesis that Antarctic poly-extreme high-latitude microbiomes harbour diverse adaptive immune systems. Our analysis reveals the prevalence of prophages in bacterial genomes (Bacteroidota and Verrucomicrobiota), suggesting the significance of lysogenic infection strategies in Antarctic soils. Furthermore, we demonstrate the presence of diverse CRISPR-Cas arrays, including Class 1 arrays (Types I-B, I-C, and I-E), alongside systems exhibiting novel gene architecture among their effector cas genes. Notably, a Class 2 system featuring type V variants lacks CRISPR arrays, encodes Cas1 and Cas2 adaptation module genes. Phylogenetic analysis of Cas12 effector proteins hints at divergent evolutionary histories compared to classified type V effectors and indicates that TnpB is likely the ancestor of Cas12 nucleases. Our findings suggest substantial novelty in Antarctic cas sequences, likely driven by strong selective pressures. These results underscore the role of viral infection as a key evolutionary driver shaping polar microbiomes.https://doi.org/10.1038/s41598-024-83942-yAdaptive immunityAntarcticaAntiphage,BacteriaCRISPR-CasEvolutionary drivers
spellingShingle Marc W. Van Goethem
Oliver K. I. Bezuidt
Rian Pierneef
Surendra Vikram
David W. Hopkins
Thomas Aspray
Grant Hall
Stephan Woodborne
Ian D. Hogg
Trent R. Northen
Weidong Kong
Daniele Daffonchio
Don A. Cowan
Yves Van de Peer
Manuel Delgado-Baquerizo
Thulani P. Makhalanyane
Novel adaptive immune systems in pristine Antarctic soils
Scientific Reports
Adaptive immunity
Antarctica
Antiphage,
Bacteria
CRISPR-Cas
Evolutionary drivers
title Novel adaptive immune systems in pristine Antarctic soils
title_full Novel adaptive immune systems in pristine Antarctic soils
title_fullStr Novel adaptive immune systems in pristine Antarctic soils
title_full_unstemmed Novel adaptive immune systems in pristine Antarctic soils
title_short Novel adaptive immune systems in pristine Antarctic soils
title_sort novel adaptive immune systems in pristine antarctic soils
topic Adaptive immunity
Antarctica
Antiphage,
Bacteria
CRISPR-Cas
Evolutionary drivers
url https://doi.org/10.1038/s41598-024-83942-y
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