Physiological basis for atmospheric methane oxidation and methanotrophic growth on air.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
16 May 2024
Historique:
received: 13 02 2024
accepted: 22 04 2024
medline: 17 5 2024
pubmed: 17 5 2024
entrez: 16 5 2024
Statut: epublish

Résumé

Atmospheric methane oxidizing bacteria (atmMOB) constitute the sole biological sink for atmospheric methane. Still, the physiological basis allowing atmMOB to grow on air is not well understood. Here we assess the ability and strategies of seven methanotrophic species to grow with air as sole energy, carbon, and nitrogen source. Four species, including three outside the canonical atmMOB group USCα, enduringly oxidized atmospheric methane, carbon monoxide, and hydrogen during 12 months of growth on air. These four species exhibited distinct substrate preferences implying the existence of multiple metabolic strategies to grow on air. The estimated energy yields of the atmMOB were substantially lower than previously assumed necessary for cellular maintenance in atmMOB and other aerobic microorganisms. Moreover, the atmMOB also covered their nitrogen requirements from air. During growth on air, the atmMOB decreased investments in biosynthesis while increasing investments in trace gas oxidation. Furthermore, we confirm that a high apparent specific affinity for methane is a key characteristic of atmMOB. Our work shows that atmMOB grow on the trace concentrations of methane, carbon monoxide, and hydrogen present in air and outlines the metabolic strategies that enable atmMOB to mitigate greenhouse gases.

Identifiants

pubmed: 38755154
doi: 10.1038/s41467-024-48197-1
pii: 10.1038/s41467-024-48197-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4151

Subventions

Organisme : Norges Forskningsråd (Research Council of Norway)
ID : 295910
Organisme : Norges Forskningsråd (Research Council of Norway)
ID : 315129

Informations de copyright

© 2024. The Author(s).

Références

Forster, P. et al. in Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (eds Masson-Delmotte, V. et al.) 923–1054 (Cambridge University Press, 2023).
Mar, K. A., Unger, C., Walderdorff, L. & Butler, T. Beyond CO2 equivalence: the impacts of methane on climate, ecosystems, and health. Environ. Sci. Policy 134, 127–136 (2022).
doi: 10.1016/j.envsci.2022.03.027
Ehhalt, D. H. The atmospheric cycle of methane. Tellus 26, 58–70 (1974).
doi: 10.1111/j.2153-3490.1974.tb01952.x
Saunois, M. et al. The Global Methane Budget 2000–2017. Earth Syst. Sci. Data. 12, 1561–1623 (2020).
doi: 10.5194/essd-12-1561-2020
Rigby, M. et al. Role of atmospheric oxidation in recent methane growth. Proc. Natl Acad. Sci. 114, 5373–5377 (2017).
pubmed: 28416657 pmcid: 5448198 doi: 10.1073/pnas.1616426114
Jackson, R. B. et al. Increasing anthropogenic methane emissions arise equally from agricultural and fossil fuel sources. Environ. Res. Lett. 15, 071002 (2020).
doi: 10.1088/1748-9326/ab9ed2
Peng, S. et al. Wetland emission and atmospheric sink changes explain methane growth in 2020. Nature 612, 477–482 (2022).
pubmed: 36517714 doi: 10.1038/s41586-022-05447-w
Ocko, I. B. & Hamburg, S. P. Climate consequences of hydrogen emissions. Atmos. Chem. Phys. 22, 9349–9368 (2022).
doi: 10.5194/acp-22-9349-2022
Dincer, I. Hydrogen 1.0: A new age. Int. J. Hydrog. Energy 48, 16143–16147 (2023).
doi: 10.1016/j.ijhydene.2023.01.124
Tate, K. R. Soil methane oxidation and land-use change—from process to mitigation. Soil Biol. Biochem. 80, 260–272 (2015).
doi: 10.1016/j.soilbio.2014.10.010
La, H., Hettiaratchi, J. P. A., Achari, G. & Dunfield, P. F. Biofiltration of methane. Bioresour. Technol. 268, 759–772 (2018).
pubmed: 30064899 doi: 10.1016/j.biortech.2018.07.043
Harriss, R. C., Sebacher, D. I. & Day, F. P. Methane flux in the Great Dismal Swamp. Nature 297, 673–674 (1982).
doi: 10.1038/297673a0
Bender, M. & Conrad, R. Kinetics of CH4 oxidation in oxic soils exposed to ambient air or high CH4 mixing ratios. FEMS Microbiol. Ecol. 10, 261–269 (1992).
doi: 10.1111/j.1574-6941.1992.tb01663.x
Knief, C., Lipski, A. & Dunfield, P. F. Diversity and activity of methanotrophic bacteria in different upland soils. Appl. Environ. Microbiol. 69, 6703–6714 (2003).
pubmed: 14602631 pmcid: 262299 doi: 10.1128/AEM.69.11.6703-6714.2003
Holmes, A. J. et al. Characterization of methanotrophic bacterial populations in soils showing atmospheric methane uptake. Appl. Environ. Microbiol. 65, 3312–3318 (1999).
pubmed: 10427012 pmcid: 91497 doi: 10.1128/AEM.65.8.3312-3318.1999
Roslev, P. & Iversen, N. Radioactive fingerprinting of microorganisms that oxidize atmospheric methane in different soils. Appl. Environ. Microbiol. 65, 4064–4070 (1999).
pubmed: 10473417 pmcid: 99742 doi: 10.1128/AEM.65.9.4064-4070.1999
Täumer, J. et al. Divergent drivers of the microbial methane sink in temperate forest and grassland soils. Glob. Chang Biol. 27, 929–940 (2021).
pubmed: 33135275 doi: 10.1111/gcb.15430
Zhao, R., Wang, H., Cheng, X., Yun, Y. & Qiu, X. Upland soil cluster γ dominates the methanotroph communities in the karst Heshang Cave. FEMS Microbiol. Ecol. 94, 192 (2018).
doi: 10.1093/femsec/fiy192
Cai, Y., Zhou, X., Shi, L. & Jia, Z. Atmospheric methane oxidizers are dominated by upland soil cluster Alpha in 20 Forest Soils of China. Micro. Ecol. 80, 859–871 (2020).
doi: 10.1007/s00248-020-01570-1
Pratscher, J., Vollmers, J., Wiegand, S., Dumont, M. G. & Kaster, A. Unravelling the identity, metabolic potential and global biogeography of the atmospheric methane‐oxidizing upland soil cluster α. Environ. Microbiol. 20, 1016–1029 (2018).
pubmed: 29314604 pmcid: 6849597 doi: 10.1111/1462-2920.14036
Täumer, J. et al. Linking transcriptional dynamics of CH4-cycling grassland soil microbiomes to seasonal gas fluxes. ISME J. 16, 1788–1797 (2022).
pubmed: 35388141 pmcid: 9213473 doi: 10.1038/s41396-022-01229-4
Deng, Y. et al. Upland soil cluster Gamma dominates methanotrophic communities in upland grassland soils. Sci. Total Environ. 670, 826–836 (2019).
pubmed: 30921716 doi: 10.1016/j.scitotenv.2019.03.299
Knief C. Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker. Front. Microbiol. 6. https://doi.org/10.3389/fmicb.2015.01346 . (2015)
Dunfield, P. F., Liesack, W., Henckel, T., Knowles, R. & Conrad, R. High-Affinity Methane Oxidation by a Soil Enrichment Culture Containing a Type II Methanotroph. Appl Environ. Microbiol. 65, 1009–1014 (1999).
pubmed: 10049856 pmcid: 91137 doi: 10.1128/AEM.65.3.1009-1014.1999
Dunfield P. F. The soil methane sink. In: Greenhouse Gas Sinks. CABI:152-170. https://doi.org/10.1079/9781845931896.0152 , (2007)
Knief, C. & Dunfield, P. F. Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ. Microbiol. 7, 1307–1317 (2005).
pubmed: 16104854 doi: 10.1111/j.1462-2920.2005.00814.x
Cai, Y., Zheng, Y., Bodelier, P. L. E., Conrad, R. & Jia, Z. Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils. Nat. Commun. 7, 11728 (2016).
pubmed: 27248847 pmcid: 4895445 doi: 10.1038/ncomms11728
Conrad, R. Soil microorganisms oxidizing atmospheric trace gases (CH4, CO, H2, NO). Indian J. Microbiol. 39, 193–203 (1999).
Tijhuis, L., Van Loosdrecht, M. C. M. & Heijnen, J. J. A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol. Bioeng. 42, 509–519 (1993).
pubmed: 18613056 doi: 10.1002/bit.260420415
Button, D. K. Differences between the kinetics of nutrient uptake by micro-organisms, growth and enzyme kinetics. Trends Biochem. Sci. 8, 121–124 (1983).
doi: 10.1016/0968-0004(83)90232-3
Degelmann, D. M., Borken, W., Drake, H. L. & Kolb, S. Different atmospheric methane-oxidizing communities in European Beech and norway spruce soils. Appl. Environ. Microbiol. 76, 3228–3235 (2010).
pubmed: 20348309 pmcid: 2869149 doi: 10.1128/AEM.02730-09
Tveit, A. T. et al. Simultaneous oxidation of atmospheric methane, carbon monoxide and hydrogen for bacterial growth. Microorganisms 9, 153 (2021).
pubmed: 33445466 pmcid: 7827875 doi: 10.3390/microorganisms9010153
Tveit, A. T. et al. Widespread soil bacterium that oxidizes atmospheric methane. Proc. Natl Acad. Sci. 116, 8515–8524 (2019).
pubmed: 30962365 pmcid: 6486757 doi: 10.1073/pnas.1817812116
Whittenbury, R., Phillips, K. C. & Wilkinson, J. F. Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol. 61, 205–218 (1970).
Dedysh, S. N. et al. Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int. J. Syst. Evol. Microbiol. 52, 251–261 (2002).
pubmed: 11837310 doi: 10.1099/00207713-52-1-251
Wartiainen, I., Hestnes, A. G., McDonald, I. R. & Svenning, M. M. Methylocystis rosea sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (78° N). Int J. Syst. Evol. Microbiol. 56, 541–547 (2006).
pubmed: 16514024 doi: 10.1099/ijs.0.63912-0
Dunfield, P. F., Belova, S. E., Vorob’ev, A. V., Cornish, S. L. & Dedysh, S. N. Methylocapsa aurea sp. nov., a facultative methanotroph possessing a particulate methane monooxygenase, and emended description of the genus Methylocapsa. Int. J. Syst. Evol. Microbiol. 60, 2659–2664 (2010).
pubmed: 20061505 doi: 10.1099/ijs.0.020149-0
Dedysh, S. N. et al. Methylocapsa palsarum sp. nov., a methanotroph isolated from a subArctic discontinuous permafrost ecosystem. Int .J. Syst. Evol. Microbiol. 65, 3618–3624 (2015).
pubmed: 26297585 doi: 10.1099/ijsem.0.000465
Bodelier, P. L. E. & Steenbergh, A. K. Interactions between methane and the nitrogen cycle in light of climate change. Curr. Opin. Environ. Sustain. 9-10, 26–36 (2014).
doi: 10.1016/j.cosust.2014.07.004
Zhang, T., Zhou, J., Wang, X. & Zhang, Y. Poly-β-hydroxybutyrate Production by Methylosinus trichosporium OB3b at Different Gas-phase Conditions. Iran. J. Biotechnol. 17, 10–16 (2019).
doi: 10.21859/ijb.1866
Greening, C. & Grinter, R. Microbial oxidation of atmospheric trace gases. Nat. Rev. Microbiol. 20, 513–528 (2022).
pubmed: 35414013 doi: 10.1038/s41579-022-00724-x
Bonk, F. et al. Determination of Microbial Maintenance in Acetogenesis and Methanogenesis by Experimental and Modeling Techniques. Front. Microbiol. 10. https://doi.org/10.3389/fmicb.2019.00166 , (2019)
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P., Huerta-Cepas, J. eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Tamura K., ed. Mol. Biol. Evol. 38:5825-5829. https://doi.org/10.1093/molbev/msab293 , (2021)
Cordero, P. R. F. et al. Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence. J. Biol. Chem. 294, 18980–18991 (2019).
pubmed: 31624148 pmcid: 6916507 doi: 10.1074/jbc.RA119.011076
Piché-Choquette, S., Khdhiri, M. & Constant, P. Dose-response relationships between environmentally-relevant H2 concentrations and the biological sinks of H2, CH4 and CO in soil. Soil Biol. Biochem. 123, 190–199 (2018).
doi: 10.1016/j.soilbio.2018.05.008
Agarwala, R. et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 46, D8–D13 (2018).
doi: 10.1093/nar/gkx1095
Culpepper, M. A. & Rosenzweig, A. C. Structure and protein-protein interactions of methanol dehydrogenase from Methylococcus capsulatus (Bath). Biochemistry 53, 6211–6219 (2014).
pubmed: 25185034 doi: 10.1021/bi500850j
Escalante-Semerena, J. C. & Wolfe, R. S. Tetrahydromethanopterin-dependent methanogenesis from non-physiological C1 donors in Methanobacterium thermoautotrophicum. J. Bacteriol. 161, 696–701 (1985).
pubmed: 3838170 pmcid: 214938 doi: 10.1128/jb.161.2.696-701.1985
Kallen, R. G. & Jencks, W. P. The mechanism of the condensation of formaldehyde with tetrahydrofolic acid. J. Biol. Chem. 241, 5851–5863 (1966).
pubmed: 5954363 doi: 10.1016/S0021-9258(18)96350-7
Marx, C. J., Chistoserdova, L. & Lidstrom, M. E. Formaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway in Methylobacterium extorquens AM1. J. Bacteriol. 185, 7160–7168 (2003).
pubmed: 14645276 pmcid: 296243 doi: 10.1128/JB.185.23.7160-7168.2003
Moon, M., Park, G. W., Lee, J. P. Y. O., Lee, J. S. & Min, K. Recent progress in formate dehydrogenase (FDH) as a non-photosynthetic CO2 utilizing enzyme: A short review. J. CO2 Utilization. 42, 101353 (2020).
doi: 10.1016/j.jcou.2020.101353
Hartmann, T. & Leimkühler, S. The oxygen‐tolerant and NAD + ‐dependent formate dehydrogenase from Rhodobacter capsulatus is able to catalyze the reduction of CO2 to formate. FEBS J. 280, 6083–6096 (2013).
pubmed: 24034888 doi: 10.1111/febs.12528
Yu, X., Niks, D., Mulchandani, A. & Hille, R. Efficient reduction of CO
pubmed: 28784661 pmcid: 5641872 doi: 10.1074/jbc.M117.785576
Crowther, G. J., Kosály, G. & Lidstrom, M. E. Formate as the Main Branch Point for Methylotrophic Metabolism in Methylobacterium extorquens AM1. J. Bacteriol. 190, 5057–5062 (2008).
pubmed: 18502865 pmcid: 2447001 doi: 10.1128/JB.00228-08
Kikuchi, G., Motokawa, Y., Yoshida, T. & Hiraga, K. Glycine cleavage system: reaction mechanism, physiological significance, and hyperglycinemia. Proc. Jpn. Acad., Ser. B. 84, 246–263 (2008).
doi: 10.2183/pjab.84.246
Claassens, N. J. et al. Engineering the Reductive Glycine Pathway: A Promising Synthetic Metabolism Approach for C1-Assimilation. In: Advances in Biochemical Engineering/Biotechnology. 180; 299−350. https://doi.org/10.1007/10_2021_181 , (2022).
Dunfield, P. F. & Conrad, R. Starvation Alters the Apparent Half-Saturation Constant for Methane in the Type II Methanotroph Methylocystis Strain LR1. Appl Environ. Microbiol. 66, 4136–4138 (2000).
pubmed: 10966442 pmcid: 92272 doi: 10.1128/AEM.66.9.4136-4138.2000
Knief, C., Kolb, S., Bodelier, P. L. E., Lipski, A. & Dunfield, P. F. The active methanotrophic community in hydromorphic soils changes in response to changing methane concentration. Environ. Microbiol. 8, 321–333 (2006).
pubmed: 16423018 doi: 10.1111/j.1462-2920.2005.00898.x
He L., et al. A methanotrophic bacterium to enable methane removal for climate mitigation. Proceedings of the National Academy of Sciences. 120. https://doi.org/10.1073/pnas.2310046120 (2023)
Button, D. K. Nutrient-limited microbial growth kinetics: overview and recent advances. Antonie Van. Leeuwenhoek. 63, 225–235 (1993).
pubmed: 8279821 doi: 10.1007/BF00871220
Nair, A. A. & Yu, F. Quantification of Atmospheric Ammonia Concentrations: A Review of Its Measurement and Modeling. Atmosphere 11, 1092 (2020).
doi: 10.3390/atmos11101092
Dabundo, R. et al. The Contamination of Commercial 15 N2 Gas Stocks with 15N–Labeled Nitrate and Ammonium and Consequences for Nitrogen Fixation Measurements. Love J. B., ed. PLoS One. 9:e110335. https://doi.org/10.1371/journal.pone.0110335 , (2014)
Couradeau, E. et al. Probing the active fraction of soil microbiomes using BONCAT-FACS. Nat. Commun. 10, 2770 (2019).
pubmed: 31235780 pmcid: 6591230 doi: 10.1038/s41467-019-10542-0
Dean, J. A. LANGE’S HANDBOOK OF CHEMISTRY. Mater. Manuf. Process. 5, 687–688 (1990).
doi: 10.1080/10426919008953291
Feijó Delgado, F. et al. Intracellular Water Exchange for Measuring the Dry Mass, Water Mass and Changes in Chemical Composition of Living Cells. Polymenis M., ed. PLoS One. 8:e67590. https://doi.org/10.1371/journal.pone.0067590 , (2013)
Cermak, N. et al. Direct single-cell biomass estimates for marine bacteria via Archimedes’ principle. ISME J. 11, 825–828 (2017).
pubmed: 27922599 doi: 10.1038/ismej.2016.161
Roller, B. R. K. et al. Single-cell mass distributions reveal simple rules for achieving steady-state growth. Ruby E. G., ed. mBio. Published online September 6, https://doi.org/10.1128/mbio.01585-23 , (2023)
Van Rossum, G. & Drake, F. L. Python 3 Reference Manual. Machine Learning 242 (2009).
The Pandas Development T, eam. pandas-dev/pandas: Pandas. Published online February https://doi.org/10.5281/zenodo.3509134 , (2020)
Hunter, J. D. Matplotlib: a 2D graphics environment. Comput Sci. Eng. 9, 90–95 (2007).
doi: 10.1109/MCSE.2007.55
Waskom, M. Seaborn: statistical data visualization. J. Open Source Softw. 6, 3021 (2021).
doi: 10.21105/joss.03021
Vallenet, D. et al. MicroScope: an integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis. Nucleic Acids Res. 48, D579–D589 (2019).
pmcid: 7145621
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
pubmed: 27348712 doi: 10.1038/nmeth.3901
R Core Team. R: A Language and Environment for Statistical Computing. Published online. https://www.R-project.org/ (2022)
Nenadic,O., Greenacre, M. Correspondence Analysis in R, with Two- and Three-dimensional Graphics: The ca Package. J. Stat. Softw. 20. https://doi.org/10.18637/jss.v020.i03 (2007)
Kassambara A., Mundt F. factoextra: Extract and Visualize the Results of Multivariate Data Analyses. Published online April 1, 2020. Accessed October 13. http://www.sthda.com/english/rpkgs/factoextra (2023)
Kanehisa, M. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).
pubmed: 10592173 pmcid: 102409 doi: 10.1093/nar/28.1.27
Altschul, S. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
pubmed: 9254694 pmcid: 146917 doi: 10.1093/nar/25.17.3389
Baty, F. et al. A Toolbox for Nonlinear Regression in R: The Package nlstools. J Stat Softw. 66. https://doi.org/10.18637/jss.v066.i05 , (2015)
Gormanns P., Reckow S., Poczatek J. C., Turck C. W., Lechene C. Segmentation of Multi-Isotope Imaging Mass Spectrometry Data for Semi-Automatic Detection of Regions of Interest. Rogers S., ed. PLoS One. 7:e30576. https://doi.org/10.1371/journal.pone.0030576 (2012)
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772 doi: 10.1038/nmeth.2019
Wickham, H. Ggplot2. Springer International Publishing; https://doi.org/10.1007/978-3-319-24277-4 , (2016)
Perez-Riverol, Y. et al. The PRIDE database resources in 2022: A hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50. https://doi.org/10.1093/nar/gkab1038 , (2022)
Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526 (1993).
pubmed: 8336541
Tamura K., Stecher G., Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Battistuzzi F. U., ed. Mol. Biol. Evol. 38:3022-3027. https://doi.org/10.1093/molbev/msab120 (2021)

Auteurs

Tilman Schmider (T)

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT-The Arctic University of Norway, 9037, Tromsø, Norway. tilman.schmider@uit.no.

Anne Grethe Hestnes (AG)

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT-The Arctic University of Norway, 9037, Tromsø, Norway.

Julia Brzykcy (J)

Department of Geomicrobiology, Institute of Microbiology, Faculty of Biology, University of Warsaw, 02-096, Warsaw, Poland.

Hannes Schmidt (H)

Department of Microbiology and Environmental Systems Science, Division of Terrestrial Ecosystem Research, University of Vienna, 1030, Vienna, Austria.

Arno Schintlmeister (A)

Department of Microbiology and Environmental Systems Science, Division of Microbial Ecology, University of Vienna, 1030, Vienna, Austria.

Benjamin R K Roller (BRK)

Department of Microbiology and Environmental Systems Science, Division of Microbial Ecology, University of Vienna, 1030, Vienna, Austria.

Ezequiel Jesús Teran (EJ)

Centro de Investigaciones en Física e Ingeniería del Centro de la Provincia de Buenos Aires (CIFICEN-UNCPBA-CONICET-CICPBA), Pinto, 399, Tandil (7000), Argentina.
Universidad Nacional del Centro de la Provincia de Buenos Aires, Facultad de Ciencias Exactas, Instituto de Física Arroyo Seco (IFAS), Pinto, 399, Tandil (7000), Argentina.

Andrea Söllinger (A)

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT-The Arctic University of Norway, 9037, Tromsø, Norway.

Oliver Schmidt (O)

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT-The Arctic University of Norway, 9037, Tromsø, Norway.

Martin F Polz (MF)

Department of Microbiology and Environmental Systems Science, Division of Microbial Ecology, University of Vienna, 1030, Vienna, Austria.

Andreas Richter (A)

Department of Microbiology and Environmental Systems Science, Division of Terrestrial Ecosystem Research, University of Vienna, 1030, Vienna, Austria.

Mette M Svenning (MM)

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT-The Arctic University of Norway, 9037, Tromsø, Norway.

Alexander T Tveit (AT)

Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT-The Arctic University of Norway, 9037, Tromsø, Norway. alexander.t.tveit@uit.no.

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