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DOE OSTI · 2531212

Novel adaptive immune systems in pristine Antarctic soils

Van Goethem, Marc W. [Univ. of Pretoria (South Africa); King Abdullah University of Science and Technology (KAUST), Thuwal (Saudi Arabia)]·Bezuidt, Oliver I. [Univ. of Pretoria (South Africa)]·Pierneef, Rian [Univ. of Pretoria (South Africa)]·Vikram, Surendra [Univ. of Pretoria (South Africa)]·Hopkins, David W. [Scotland’s Rural College, Edinburgh (United Kingdom)]·Aspray, Thomas [Heriot-Watt Univ., Edinburgh (United Kingdom)]·Hall, Grant [Univ. of Pretoria (South Africa)]·Woodborne, Stephan [iThemba LABS, Johannesburg (South Africa)]·Hogg, Ian D. [Univ. of Waikato (New Zealand)]·Northen, Trent R. [Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)]·Kong, Weidong [Chinese Academy of Sciences (CAS), Beijing (China)]·Daffonchio, Daniele [King Abdullah University of Science and Technology (KAUST), Thuwal (Saudi Arabia)]·Cowan, Don A. [Univ. of Pretoria (South Africa)]·Van de Peer, Yves [Univ. of Pretoria (South Africa); Ghent Univ. (Belgium); Center for Plant Systems Biology, Ghent (Belgium)]·Delgado-Baquerizo, Manuel [Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS) (Spain); Consejo Superior de Investigaciones Cientificas (CSIC), Seville (Spain); Universidad Pablo de Olavide, Seville (Spain)]·Makhalanyane, Thulani P. [Univ. of Pretoria (South Africa); Stellenbosch University (South Africa)]
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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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59 BASIC BIOLOGICAL SCIENCESAdaptive immunityAntarctica, AntiphageBacteriaCRISPR-CasEvolutionary drivers

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Van Goethem, Marc W. [Univ. of Pretoria (South Africa); King Abdullah University of Science and Technology (KAUST), Thuwal (Saudi Arabia)], Bezuidt, Oliver I. [Univ. of Pretoria (South Africa)], Pierneef, Rian [Univ. of Pretoria (South Africa)], Vikram, Surendra [Univ. of Pretoria (South Africa)], Hopkins, David W. [Scotland’s Rural College, Edinburgh (United Kingdom)], Aspray, Thomas [Heriot-Watt Univ., Edinburgh (United Kingdom)], Hall, Grant [Univ. of Pretoria (South Africa)], Woodborne, Stephan [iThemba LABS, Johannesburg (South Africa)], Hogg, Ian D. [Univ. of Waikato (New Zealand)], Northen, Trent R. [Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)], Kong, Weidong [Chinese Academy of Sciences (CAS), Beijing (China)], Daffonchio, Daniele [King Abdullah University of Science and Technology (KAUST), Thuwal (Saudi Arabia)], Cowan, Don A. [Univ. of Pretoria (South Africa)], Van de Peer, Yves [Univ. of Pretoria (South Africa); Ghent Univ. (Belgium); Center for Plant Systems Biology, Ghent (Belgium)], Delgado-Baquerizo, Manuel [Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS) (Spain); Consejo Superior de Investigaciones Cientificas (CSIC), Seville (Spain); Universidad Pablo de Olavide, Seville (Spain)], Makhalanyane, Thulani P. [Univ. of Pretoria (South Africa); Stellenbosch University (South Africa)]. 2025-01-18. Novel adaptive immune systems in pristine Antarctic soils. https://doi.org/10.1038/s41598-024-83942-y

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