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Exploring the upper pH limits of nitrite oxidation: diversity, ecophysiology, and adaptive traits of haloalkalitolerant Nitrospira
Document Type
Article
Source
The ISME Journal; December 2020, Vol. 14 Issue: 12 p2967-2979, 13p
Subject
Language
ISSN
17517362; 17517370
Abstract
Nitrite-oxidizing bacteria of the genus Nitrospiraare 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 Nitrospirathat 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 were Nitrospirapopulations detected, but they were also considerably diverse with presence of members from  Nitrospiralineages I, II and IV. Furthermore, the ability of Nitrospiraenrichment cultures to oxidize nitrite at neutral to highly alkaline pH of 10.5 was demonstrated. Metagenomic analysis of a newly enriched Nitrospiralineage 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 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 Nitrospiracope with strongly fluctuating pH and salinity conditions and expand our knowledge of nitrogen cycling in extreme habitats.