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

Anne Daebeler*, Katharina Kitzinger, Hanna Koch, Craig W. Herbold, Michaela Steinfeder, Jasmin Schwarz, Thomas Zechmeister, Søren M. Karst, Mads Albertsen, Per H. Nielsen, Michael Wagner, Holger Daims


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Nitrite-oxidizing bacteria of the genus Nitrospira are 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, haloalkalitolerant Nitrospira that drive nitrite oxidation at exceptionally high pH. Nitrospira distribution, 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 were Nitrospira populations detected, but they were also considerably diverse with presence of members from Nitrospira lineages I, II and IV. Furthermore, the ability of Nitrospira enrichment cultures to oxidize nitrite at neutral to highly alkaline pH of 10.5 was demonstrated. Metagenomic analysis of a newly enriched Nitrospira lineage IV species, “Candidatus Nitrospira 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 in Nitrospira. 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 how Nitrospira cope with strongly fluctuating pH and salinity conditions and expand our knowledge of nitrogen cycling in extreme habitats.

TidsskriftISME Journal
Udgave nummer12
Sider (fra-til)2967-2979
Antal sider13
StatusUdgivet - 1 dec. 2020

Bibliografisk note

Funding Information:
Acknowledgements The authors thank Beate Pitzl from the Biological Station WasserCluster Lunz, Austria for chemical analysis and Zsófia Horváth for help with sample collection. We are further grateful to Sebastian Lücker for developing and sharing a Nitrospina nxrB reverse primer sequence. Queralt Güell-Bujon is acknowledged for maintaining and optimizing growth conditions of enrichments. This research was supported by the Austrian Science Fund (FWF) grants T938 (to AD), and P25231-B21 and P27319-B21 (both to HD).

Publisher Copyright:
© 2020, The Author(s).


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