Abstract

The recent discovery of comammox Nitrospira as complete nitrifiers has fundamentally renewed perceptions of nitrogen cycling in natural and engineered systems, yet little is known about the environmental controls on these newly recognized bacteria. Based on improved phylogenetic resolution through successful assembly of ten novel genomes (71–96% completeness), we provided the first biogeographic patterns for planktonic and benthic comammox Nitrospira in the Yangtze River over a 6030 km continuum. Our study revealed the widespread distributions and relative abundance of comammox Nitrospira in this large freshwater system, constituting 30 and 46% of ammonia-oxidizing prokaryotes (AOPs) and displaying 30.4- and 17.9-fold greater abundances than canonical Nitrospira representatives in water and sediments, respectively. Comammox Nitrospira contributed more to nitrifier abundances (34–87% of AOPs) in typical oligotrophic environments with a higher pH and lower temperature, particularly in the plateau (clade B), mountain and foothill (clade A) areas of the upper reach. The dominant position of planktonic comammox Nitrospira was replaced by canonical Nitrospira sublineages I/II and ammonia-oxidizing bacteria from the plateau to downstream plain due to environmental selection, while the dissimilarity of benthic comammox Nitrospira was moderately associated with geographic distance. A substantial decrease (83%) in benthic comammox Nitrospira abundance occurred immediately downstream of the Three Gorges Dam, consistent with a similarly considerable decrease in overall sediment bacterial taxa. Together, this study highlights the previously unrecognized dominance of comammox Nitrospira in major river systems and underlines the importance of revisiting the distributions of and controls on nitrification processes within global freshwater environments.

Highlights

  • These authors contributed : Shufeng Liu, Haiying Wang

  • We found that the abundance ratios of comammox Nitrospira and AOB or canonical Nitrospira sublineages I/II were strongly and negatively correlated with NH3-N, total nitrogen (TN), total organic carbon (TOC), or total phosphorus (TP) (Spearman’s r = −0.40 to −0.70, p = 0.0001–0.0406), whereas the abundance ratio of comammox Nitrospira and ammonia-oxidizing archaea (AOA) was not significantly correlated with NH3-N, TOC, and TP (p = 0.10–0.35) and less significantly related to TN when comparing Spearman’s correlation coefficients (Fig. 5)

  • Based on the improved phylogenetic resolution achieved by assembling ten novel metagenomeassembled genomes (MAGs), we provided the first biogeography of planktonic and benthic comammox Nitrospira in the Yangtze River over a 6030 km continuum

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Summary

Methods

DNA extraction, and metagenomic shotgun sequencingThe Yangtze River originates from the Tangula Mountains and flows into the East China Sea, supporting 588 million people in China [23]. In October 2014, paired surface water and sediments were sampled and pretreated synchronously at 24 national hydrologic sites along the mainstream, from Shigu (SG) in the upper reach to Xuliujing (XLJ) in the estuary (Fig. 1; Supplementary Table S1). In July 2017, additional synchronous sampling was implemented at three national hydrologic sites Tuotuohe (TTH), Tongtianhe (TOTH) and Zhimenda (ZMD) in the source region of the Yangtze River located on the Qinghai-Tibetan Plateau. Genomic DNA was extracted from each sample, and a paired-end strategy (2 × 150 bp with an insert size of 300 bp) was employed for shotgun sequencing on an Illumina HiSeq 4000 platform (Majorbio Company, Shanghai, China) (Supplementary Information). A total of 30 water and 32 sediment metagenomic datasets were acquired

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