Comammox Nitrospira within the Yangtze River continuum: community, biogeography, and ecological drivers

Kuypers MMM, Marchant HK, Kartal B. The microbial nitrogen-cycling network. Nat Rev Microbiol. 2018;16:263–76.

CAS  PubMed  Google Scholar 

Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437:543–6.

PubMed  Google Scholar 

Teske A, Alm E, Regan JM, Toze S, Rittmann BE, Stahl DA. Evolutionary relationships among ammonia-and nitrite-oxidizing bacteria. J Bacteriol. 1994;176:6623–30.

CAS  PubMed  PubMed Central  Google Scholar 

Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, et al. Complete nitrification by Nitrospira bacteria. Nature. 2015;528:504–9.

CAS  PubMed  PubMed Central  Google Scholar 

van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, et al. Complete nitrification by a single microorganism. Nature. 2015;528:555–9.

PubMed  PubMed Central  Google Scholar 

Daims H, Nielsen JL, Nielsen PH, Schleifer KH, Wagner M. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl Environ Microbiol. 2001;67:5273–84.

CAS  PubMed  PubMed Central  Google Scholar 

Palomo A, Pedersen AG, Fowler SJ, Dechesne A, Sicheritz-Pontén T, Smets BF. Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME J. 2018;12:1779–93.

PubMed  PubMed Central  Google Scholar 

Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, et al. Comammox in drinking water systems. Water Res. 2017;116:332–41.

CAS  PubMed  Google Scholar 

Pinto AJ, Marcus DN, Ijaz UZ, Bautista-de lose Santos QM, Dick GJ, Raskin L. Metagenomic evidence for the presence of comammox Nitrospira-like bacteria in a drinking water system. mSphere. 2016;1:e00054–15.

PubMed  Google Scholar 

Camejo PY, Santo Domingo J, McMahon KD, Noguera DR. Genome-enabled insights into the ecophysiology of the comammox bacterium “Candidatus Nitrospira nitrosa”. mSystems. 2017;2:e00059–17.

CAS  PubMed  PubMed Central  Google Scholar 

Lawson CE, Lücker S. Complete ammonia oxidation: an important control on nitrification in engineered ecosystems? Curr Opin Biotechnol. 2018;50:158–65.

CAS  PubMed  Google Scholar 

Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel MAHJ, Daebeler A, et al. AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front Microbiol. 2017;8:1508.

PubMed  PubMed Central  Google Scholar 

Zhao Z, Huang G, He S, Zhou N, Wang M, Dang C, et al. Abundance and community composition of comammox bacteria in different ecosystems by a universal primer set. Sci Total Environ. 2019;691:146–55.

CAS  PubMed  Google Scholar 

Palomo A, Dechesne A, Smets BF. Genomic profiling of Nitrospira species reveals ecological success of comammox Nitrospira. bioRxiv. 2019:612226.

Yu C, Hou L, Zheng Y, Liu M, Yin G, Gao J, et al. Evidence for complete nitrification in enrichment culture of tidal sediments and diversity analysis of clade a comammox Nitrospira in natural environments. Appl Microbiol Biotechnol. 2018;102:1–15.

Google Scholar 

Shi X, Hu HW, Wang J, He JZ, Zheng C, Wan X, et al. Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition. Soil Biol Biochem. 2018;126:114–22.

CAS  Google Scholar 

Wang Y, Ni J, Yue Y, Li J, Borthwick AGL, Cai X, et al. Solving the mystery of vanishing rivers in China. Natl Sci Rev. 2019;6:1239–46.

Google Scholar 

Li L, Ni J, Chang F, Yue Y, Frolova N, Magritsky D, et al. Global trends in water and sediment fluxes of the world’s large rivers. Sci Bull. 2020;65:62–9.

Google Scholar 

Wang Y, Chen X, Borthwick AGL, Li T, Liu H, Yang S, et al. Sustainability of global Golden Inland Waterways. Nat Commun. 2020;11:1553.

CAS  PubMed  PubMed Central  Google Scholar 

Lansdown K, McKew BA, Whitby C, Heppell CM, Dumbrell AJ, Binley A, et al. Importance and controls of anaerobic ammonium oxidation influenced by riverbed geology. Nat Geosci. 2016;9:357–60.

CAS  Google Scholar 

Huang S, Chen C, Jaffé PR. Seasonal distribution of nitrifiers and denitrifiers in urban river sediments affected by agricultural activities. Sci Total Environ. 2018;642:1282–91.

CAS  PubMed  Google Scholar 

Black EM, Just CL. The genomic potentials of NOB and comammox Nitrospira in river sediment are impacted by native freshwater mussels. Front Microbiol. 2018;9:2061.

PubMed  PubMed Central  Google Scholar 

Qu S, Wang L, Lin A, Zhu H, Yuan M. What drives the vegetation restoration in Yangtze River basin, China: climate change or anthropogenic factors? Ecol Indic. 2018;90:438–50.

Google Scholar 

Zhao L, Li W, Lin L, Guo W, Zhao W, Tang X, et al. Field investigation on river hydrochemical characteristics and larval and juvenile fish in the source region of the Yangtze River. Water. 2019;11:1342.

CAS  Google Scholar 

Wang J, Liu Q, Zhao X, Borthwick AGL, Liu Y, Chen Q, et al. Molecular biogeography of planktonic and benthic diatoms in the Yangtze River. Microbiome. 2019;7:153.

PubMed  PubMed Central  Google Scholar 

Liu T, Zhang AN, Wang J, Liu S, Jiang X, Dang C, et al. Integrated biogeography of planktonic and sedimentary bacterial communities in the Yangtze River. Microbiome. 2018;6:16.

CAS  PubMed  PubMed Central  Google Scholar 

Chen L, Liu S, Chen Q, Zhu G, Wu X, Wang J, et al. Anammox response to natural and anthropogenic impacts over the Yangtze River. Sci Total Environ. 2019;665:171–80.

CAS  PubMed  Google Scholar 

Patel RK, Jain M. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One. 2012;7:e30619.

CAS  PubMed  PubMed Central  Google Scholar 

Chen B, Yuan K, Chen X, Yang Y, Zhang T, Wang Y, et al. Metagenomic analysis revealing antibiotic resistance genes (ARGs) and their genetic compartments in the Tibetan environment. Environ Sci Technol. 2016;50:6670–9.

CAS  PubMed  Google Scholar 

Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, et al. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature. 2011;480:368–71.

CAS  PubMed  Google Scholar 

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.

CAS  PubMed  PubMed Central  Google Scholar 

Yang Y, Jiang XT, Zhang T. Evaluation of a hybrid approach using UBLAST and BLASTX for metagenomic sequences annotation of specific functional genes. PLoS One. 2014;9:e110947.

PubMed  PubMed Central  Google Scholar 

Peng Y, Leung HCM, Yiu SM, Chin FYL. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics. 2012;28:1420–8.

CAS  PubMed  Google Scholar 

Ma L, Xia Y, Li B, Yang Y, Li LG, Tiedje JM, et al. Metagenomic assembly reveals hosts of antibiotic resistance genes and the shared resistome in pig, chicken, and human feces. Environ Sci Technol. 2015;50:420–7.

CAS  PubMed  Google Scholar 

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.

CAS  PubMed  PubMed Central  Google Scholar 

Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165.

PubMed  PubMed Central  Google Scholar 

Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

CAS  PubMed  PubMed Central  Google Scholar 

Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol. 2013;31:533–8.

CAS  PubMed  Google Scholar 

Bosi E, Donati B, Galardini M, Brunetti S, Sagot MF, Lió P, et al. MeDuSa: a multi-draft based scaffolder. Bioinformatics. 2015;31:2443–51.

CAS  PubMed  Google Scholar 

Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol. 2012;13:R56.

PubMed  PubMed Central  Google Scholar 

Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom. 2011;12:402.

CAS  Google Scholar 

Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC. Bioinform. 2010;11:119.

Google Scholar 

Darling AE, Jospin G, Lowe E, Matsen FA IV, Bik HM, Eisen JA. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ. 2014;2:e243.

PubMed  PubMed Central  Google Scholar 

Lee I, Kim YO, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol. 2016;66:1100–3.

CAS  PubMed  Google Scholar 

Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package version 2.5-1. https://CRAN.R-project.org/package=vegan.

Jurasinski G. simba: A Collection of functions for similarity analysis of vegetation data. R package version 0.3-5. https://CRAN.R-project.org/package=simba.

Harrell Jr FE, Dupont C. Hmisc: harrell miscellaneous. R package version 4.1-1. https://CRAN.R-project.org/package=Hmisc.

Wickham H, Chang W. ggplot2: An implementation of the Grammar of Graphics. R package version 3.1.1. http://CRAN.R-project.org/package=ggplot2.

Wang XB, Lü XT, Yao J, Wang ZW, Deng Y, Cheng WX, et al. Habitat-specific patterns and drivers of bacterial β-diversity in China’s drylands. ISME J 2017;11:1345–58.

PubMed  PubMed Central  Google Scholar 

Wu L, Ning D, Zhang B, Li Y, Zhang P, Shan X, et al. Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nat Microbiol. 2019;4:1183–95.

CAS  PubMed  Google Scholar 

Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature. 2017;549:269–72.

CAS  PubMed  PubMed Central  Google Scholar 

Fang G, Rocha EPC, Danchin A. Persistence drives gene clustering in bacterial genomes. BMC Genom. 2008;9:4.

Google Scholar 

Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA. 2009;106:19126–31.

CAS  PubMed  Google Scholar 

Costa E, Pérez J, Kreft JU. Why is metabolic labour divided in nitrification? Trends Microbiol. 2006;14:213–9.

CAS  PubMed  Google Scholar 

Zhou J, Ning D. Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev. 2017;81:e00002–17.

PubMed  PubMed Central  Google Scholar 

Daims H, Lücker S, Wagner M. A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol. 2016;24:699–712.

CAS  PubMed  PubMed Central  Google Scholar 

Kits KD, Jung MY, Vierheilig J, Pjevac P, Sedlacek CJ, Liu S, et al. Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata. Nat Commun. 2019;10:1836.

PubMed  PubMed Central  Google Scholar 

Palomo A, Fowler SJ, Gülay A, Rasmussen S, Sicheritz-Ponten T, Smets BF. Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology of Nitrospira spp. ISME J. 2016;10:2569–81.

CAS  PubMed  PubMed Central  Google Scholar 

Bartelme RP, McLellan SL, Newton RJ. Freshwater recirculating aquaculture system operations drive biofilter bacterial community shifts around a stable nitrifying consortium of ammonia-oxidizing archaea and comammox Nitrospira. Front Microbiol. 2017;8:101.

PubMed  PubMed Central  Google Scholar 

Fowler SJ, Palomo A, Dechesne A, Mines PD, Smets BF. Comammox Nitrospira are abundant ammonia oxidizers in diverse groundwater-fed rapid sand filter communities. Environ Microbiol. 2018;20:1002–15.

CAS  PubMed  Google Scholar 

Kolmakova OV, Gladyshev MI, Rozanov AS, Peltek SE, Trusova MY. Spatial biodiversity of bacteria along the largest Arctic river determined by next-generation sequencing. FEMS Microbiol Ecol. 2014;89:442–50.

CAS  PubMed  Google Scholar 

Bell T. Experimental tests of the bacterial distance-decay relationship. ISME J. 2010;4:1357–65.

PubMed  Google Scholar 

Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206.

PubMed  Google Scholar 

Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343–66.

Google Scholar 

Huang L, Dong H, Jiang H, Wang S, Yang J. Relative importance of advective flow versus environmental gradient in shaping aquatic ammonium oxidizers near the Three Gorges Dam of the Yangtze River, China. Environ Microbiol Rep. 2016;8:667–74.

PubMed  Google Scholar 

Battin TJ, Besemer K, Bengtsson MM, Romani AM, Packmann AI. The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol. 2016;14:251–63.

CAS  PubMed  Google Scholar 

Hu HW, He JZ. Comammox—a newly discovered nitrification process in the terrestrial nitrogen cycle. J Soil Sediment. 2017;17:2709–17.

CAS  Google Scholar 

Lee DH, Choi SL, Rha E, Kim SJ, Yeom SJ, Moon JH, et al. A novel psychrophilic alkaline phosphatase from the metagenome of tidal flat sediments. BMC Biotechnol. 2015;15:1.

PubMed  PubMed Central  Google Scholar 

Chen X, Yan Y, Fu R, Dou X, Zhang E. Sediment transport from the Yangtze River, China, into the sea over the Post-Three Gorge Dam Period: a discussion. Quatern Int. 2008;186:55–64.

Google Scholar 

Tao K, Liu Y, Ke T, Zhang Y, Xiao L, Li S, et al. Patterns of bacterial and archaeal communities in sediments in response to dam construction and sewage discharge in Lhasa River. Ecotoxicol Environ Saf. 2019;178:195–201.

CAS  PubMed  Google Scholar 

Orell A, Fröls S, Albers SV. Archaeal biofilms: the great unexplored. Annu Rev Microbiol. 2013;67:337–54.

CAS  PubMed  Google Scholar 

Stahl DA, de la Torre JR. Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol. 2012;66:83–101.

CAS  PubMed  Google Scholar 

Quince C, Walker AW, Simpson JT, Loman NJ, Segata N. Shotgun metagenomics, from sampling to analysis. Nat Biotechnol. 2017;35:833–44.

CAS  PubMed  Google Scholar 

Ju F, Zhang T. Experimental design and bioinformatics analysis for the application of metagenomics in environmental sciences and biotechnology. Environ Sci Technol. 2015;49:12628–40.

CAS  PubMed  Google Scholar 

Alneberg J, Bjarnason BS, de Bruijn I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144–6.

CAS  PubMed  Google Scholar