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Exploring the upper pH limits of nitrite oxidation: diversity, ecophysiology, and adaptive traits of haloalkalitolerantNitrospira

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Kitzinger,  Katharina
Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Citation

Daebeler, A., Kitzinger, K., Koch, H., Herbold, C. W., Steinfeder, M., Schwarz, J., et al. (2020). Exploring the upper pH limits of nitrite oxidation: diversity, ecophysiology, and adaptive traits of haloalkalitolerantNitrospira. The ISME Journal, 14(12), 2967-2979. doi:10.1038/s41396-020-0724-1.


Cite as: http://hdl.handle.net/21.11116/0000-0007-CD5A-E
Abstract
Nitrite-oxidizing bacteria of the genusNitrospiraare key players of the biogeochemical nitrogen cycle. However, little is known about their occurrence and survival strategies in extreme pH environments. Here, we report on the discovery of physiologically versatile, haloalkalitolerantNitrospirathat drive nitrite oxidation at exceptionally high pH.Nitrospiradistribution, diversity, and ecophysiology were studied in hypo- and subsaline (1.3-12.8 g salt/l), highly alkaline (pH 8.9-10.3) lakes by amplicon sequencing, metagenomics, and cultivation-based approaches. Surprisingly, not only wereNitrospirapopulations detected, but they were also considerably diverse with presence of members from Nitrospiralineages I, II and IV. Furthermore, the ability ofNitrospiraenrichment cultures to oxidize nitrite at neutral to highly alkaline pH of 10.5 was demonstrated. Metagenomic analysis of a newly enrichedNitrospiralineage IV species, "CandidatusNitrospira alkalitolerans", revealed numerous adaptive features of this organism to its extreme environment. Among them were a sodium-dependent N-type ATPase and NADH:quinone oxidoreductase next to the proton-driven forms usually found inNitrospira. Other functions aid in pH and cation homeostasis and osmotic stress defense. "Ca. Nitrospira alkalitolerans" also possesses group 2a and 3b [NiFe] hydrogenases, suggesting it can use hydrogen as alternative energy source. These results reveal howNitrospiracope with strongly fluctuating pH and salinity conditions and expand our knowledge of nitrogen cycling in extreme habitats.