Niche specialization and ecophysiological adaptation strategies of salt-tolerant nitrite oxidizers in soil

Members of genus Nitrospira represent the most diverse nitrite-oxidizing bacteria (NOB) and are ubiquitous in terrestrial ecosystems, which complete the nitrification process by converting nitrite to nitrate. NOB has shown physiological adaptation to a wide range of environmental conditions, including extreme pH and salinity. However, little is known about their ecological performances and adaptation features in salt-affected soils. Here, we revealed the genomic adaptations of active NOB in a saline-sodic soil (solonetz) with high Na + stress (20.9 cmol c exchangeable Na + kg −1 soil) and pH (9.64), using approaches of 13 C-DNA stable-isotope tracing and amplicon-based and metagenomic sequencing. Two novel Nitrospira lineage IV–affiliated genomes (“ Nitrospira sp. Sol IV1” and “ Nitrospira sp. Sol IV2”) were identified by 13 C-labeled metagenomic assemble and represented the primary contributors in the solonetz. The genomic analysis of Sol IV1 and IV2 revealed various adaptive strategies for salt tolerance, including direct Na + extrusion/H + import, compatible-solute accumulations, and highly efficient energy supply. In contrast, the Nitrospira lineages I and V with much less salt-adaptation features co-dominated the nitrite oxidation in an adjacent nonsaline farmland soil converted from the solonetz, indicating salt tolerance–based niche differentiation of distinct soil NOB phylotypes. This study provides the first direct evidence for autotrophic nitrite oxidation of Nitrospira lineage IV in soil and their critical ecological role in regulating nitrogen (N) cycling in hypersaline terrestrial ecosystems, expanding our understanding of the habitat occupation range and metabolic versatility of nitrifying communities.