In-situ expressions of comammox Nitrospira along the Yangtze River

Shufeng Liu; Hetong Cai; Jiawen Wang; Haiying Wang; Tong Zheng; Qian Chen; Jinren Ni

doi:10.1016/j.watres.2021.117241

In-situ expressions of comammox Nitrospira along the Yangtze River

Water Res. 2021 Jul 15:200:117241. doi: 10.1016/j.watres.2021.117241. Epub 2021 May 13.

Authors

Shufeng Liu¹, Hetong Cai¹, Jiawen Wang¹, Haiying Wang², Tong Zheng³, Qian Chen⁴, Jinren Ni⁵

Affiliations

¹ Key Laboratory of Water and Sediment Sciences, Ministry of Education, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing 100871, China.
² Key Laboratory of Water and Sediment Sciences, Ministry of Education, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China.
³ Key Laboratory of Water and Sediment Sciences, Ministry of Education, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing 100871, China; South China Institute of Environmental Sciences, Ministry of Environmental Protection (MEP), Guangzhou 510655, China.
⁴ Key Laboratory of Water and Sediment Sciences, Ministry of Education, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing 100871, China; State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China.
⁵ Key Laboratory of Water and Sediment Sciences, Ministry of Education, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing 100871, China; State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China. Electronic address: jinrenni@pku.edu.cn.

PMID: 34051458
DOI: 10.1016/j.watres.2021.117241

Abstract

The recent discovery of comammox Nitrospira as complete nitrifiers has significantly enriched our understanding on the nitrogen cycle, yet little is known about their metabolic transcripts in natural aquatic ecosystems. Using the genome-centric metatranscriptomics, we provided the first in-situ expression patterns of comammox Nitrospira along the Yangtze River. Our study confirmed widespread expressions of comammox Nitrospira, with the highest transcription accounting for 33.3% and 63.8% of amoA and nxrAB genes expressed in ammonia-oxidizing prokaryotes (AOPs) and Nitrospira sublineages I/II, respectively. Moreover, comammox two clades differed in nitrification, with clade A acting as the dominator to ammonia oxidation in comammox, and clade B contributing more transcripts to nitrite oxidation than to ammonia oxidation. Compared to canonical Nitrospira, comammox community had lower expressions of ammonia/nitrite transporters and nitrogen assimilatory genes, but far higher expressions in urea transport and hydrolysis, facilitating to derivation of ammonia and energy mainly through intracellular ureolytic metabolism. This suggests no need for "reciprocal-feeding" between canonical Nitrospira and AOPs in a natural river. Aerobic mixotrophy of comammox bacteria was suggested by expressions of genes coding for respiratory complexes I-V, oxidative/reductive TCA cycle, oxygen stress defenses, and transport/catabolism of simple carbohydrates and low-biosynthetic-cost amino acids. Intriguingly, significant positive correlations among expressions of ammonia monooxygenases, hydroxylamine dehydrogenase and copper-dependent nitrite reductase indicated that comammox Nitrospira had the potential of converting nitrite to nitric oxide accompanied by ammonia oxidation under low-C/N and aerobic conditions, while gene expressions in this pathway were significantly and positively associated with pH. Overall, this study illustrated novel transcriptional characteristics of comammox Nitrospira, and highlighted the necessity of reassessing their contributions to biogeochemical carbon and nitrogen cycling with perspective of in-situ meta-omics as well as culture experiments.

Keywords: Yangtze River; comammox Nitrospira; complete nitrifiers; environmental drivers; genome-centric metatranscriptomics; in-situ expression patterns.

MeSH terms

Ammonia
Archaea
Bacteria / genetics
Ecosystem*
Nitrification
Oxidation-Reduction
Phylogeny
Rivers*

Substances

Ammonia