Skip to main content
Log in

Pangenome-driven insights into nitrogen metabolic characteristics of Citrobacter portucalensis strain AAK_AS5 associated with wastewater nitrogen removal

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Nitrogen metabolism in the genus Citrobacter is very poorly studied despite its several implications in wastewater treatment. In the current study, Citrobacter portucalensis strain AAK_AS5 was assessed for remediation of simulated wastewater supplemented with different inorganic nitrogen sources. Combination of (NH4)2SO4 with KNO3 was the most preferred for achieving high growth density followed by (NH4)2SO4 and KNO3 alone. This was in agreement with highest ammonical nitrogen removal of 92.9% in the presence of combined nitrogen sources and the corresponding nitrate nitrogen removal of 93% in the presence of KNO3. Furthermore, these removal capacities were validated by investigating the uniqueness and the spread of metabolic features through pan-genomic approach that revealed the largest number of unique genes (2097) and accessory genes (705) in strain AAK_AS5. Of the total 44 different types of nitrogen metabolism-related genes, 39 genes were associated with the core genome, while 5 genes such as gltInasAnasRnrtA, and ntrC uniquely belonged to the accessory genome. Strain AAK_AS5 possessed three major nitrate removal pathways viz., assimilatory and dissimilatory nitrate reduction to ammonia (ANRA & DNRA), and denitrification; however, the absence of nitrification was compensated by ammonia assimilation catalyzed by gene products of the GDH and GS-GOGAT pathways. narGHIJ encoding the respiratory nitrate reductase was commonly identified in all the studied genomes, while genes such as nirK, norB, and nosZ were uniquely present in the strain AAK_AS5 only. A markedly different genetic content and metabolic diversity between the strains reflected their adaptive evolution in the environment thus highlighting the significance of C. portucalensis AAK_AS5 for potential application in nitrogen removal from wastewater.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

This Whole Genome Shotgun project has been deposited in GenBank under the accession number SDHR00000000.

References

  • An S-Y, Min S-K, Cha I-H, Choi Y-L, Cho Y-S, Kim C-H, Lee Y-CJBl. (2002) Decolorization of triphenylmethane and azo dyes by Citrobacter sp. Biotechnol Lett 24:1037–1040

    Article  CAS  Google Scholar 

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available online at http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accessed 21 Dec 2021

  • Ankrah NY, Luan J, Douglas AE (2017) Cooperative metabolism in a three-partner insect-bacterial symbiosis revealed by metabolic modeling. J Bacteriol 199(15):e00872-16

  • APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association and Water Environmental Federation, Washington, DC

  • Arumugaperumal A, Paul S, Lathakumari S, Balasubramani R, Sivasubramaniam S (2020) The draft genome of a new Verminephrobacter eiseniae strain: a nephridial symbiont of earthworms. Ann Microbiol 70:1–18

    Article  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:1–15

    Article  Google Scholar 

  • Bagchi S, Biswas R, Nandy T (2012) Autotrophic ammonia removal processes: ecology to technology. Crit Rev Environ Sci Technol 42:1353–1418

    Article  CAS  Google Scholar 

  • Barathi S, Meng Y, Yu Z, Ni S-Q, Meng F (2021) Roles of nitrite in mediating the composition and metacommunity of multispecies biofilms. J Water Process Eng 40:101764

    Article  Google Scholar 

  • Bhandari VM, Sorokhaibam LG, Ranade VV (2016) Industrial wastewater treatment for fertilizer industry—a case study. Desalin Water Treat 57(57):27934–27944

    CAS  Google Scholar 

  • Bock E, Schmid I, Stüven R, Zart D (1995) Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium or hydrogen as electron donors and nitrite as electron acceptor. Arch Microbiol 163(1):16–20

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:1–6

    Article  Google Scholar 

  • Burkovski A (2003) Ammonium assimilation and nitrogen control in Corynebacterium glutamicum and its relatives: an example for new regulatory mechanisms in actinomycetes. FEMS Microbiol Rev 27:617–628

    Article  CAS  PubMed  Google Scholar 

  • Canfield DE, Glazer AN, Falkowski PGJs. (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196

    Article  CAS  PubMed  Google Scholar 

  • Chan GF, Gan HM, Rashid NAA (2012) Genome sequence of Citrobacter sp. strain A1, a dye-degrading bacterium. Am Soc Microbiol 194:5485–5486

    CAS  Google Scholar 

  • Chaudhari NM, Gupta VK, Dutta C (2016) BPGA-an ultra-fast pan-genome analysis pipeline. Sci Rep 6:1–10

    Article  Google Scholar 

  • Chen H, Wang Y, Zhang J, Chen Y, Wu M (2017) Isolation and identification of Citrobacter spp. from the intestine of Procambarus clarkii. J Fish Res 2:1–6

    CAS  Google Scholar 

  • Cho G-S, Stein M, Bockelmann W, Neve H, Brinks E, Franz CM (2018) Draft genome sequence of Citrobacter gillenii MBT-C3, isolated from Lamb’s lettuce. Microbiol Resour Announc 7:e01177-e11118

    Article  PubMed  PubMed Central  Google Scholar 

  • Costa SS, Guimarães LC, Silva A, Soares SC, Baraúna RA (2020) First steps in the analysis of prokaryotic pan-genomes. Bioinform Biol Insights 14:1177932220938064

    Article  PubMed  PubMed Central  Google Scholar 

  • de Los Santos-Villalobos S, Kremer J, Parra-Cota F, Hayano-Kanashiro A, García-Ortega L, Gunturu S, Tiedje J, He S, Peña-Cabriales J (2018) Draft genome of the fungicidal biological control agent Burkholderia anthina strain XXVI. Arch Microbiol 200:803–810

    Article  PubMed  Google Scholar 

  • Dey S, Haripavan N, Basha S, Babu G (2021) Removal of ammonia and nitrates from contaminated water by using solid waste bio-adsorbents. Curr Res Chem Biol 1:100005

    Article  CAS  Google Scholar 

  • Duceppe M-O, Phipps-Todd B, Carrillo C, Huang H (2019) Draft genome sequences of eight Canadian Citrobacter braakii and Citrobacter freundii strains. Microbiol Resour Announc 8:e00273-e1219

    Article  PubMed  PubMed Central  Google Scholar 

  • Egli K, Fanger U, Alvarez PJ, Siegrist H, van der Meer JR, Zehnder HAJ (2001) Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol 175(3):198–207

    Article  CAS  PubMed  Google Scholar 

  • French J, Turner G, Bradbury JJM (1976) Nitrogen fixation by bacteria from the hindgut of termites. Microbiology 95:202–206

    CAS  Google Scholar 

  • Frias JE, Flores E, Herrero A (1997) Nitrate assimilation gene cluster from the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 179:477–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169–4182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta RK, Poddar BJ, Nakhate SP, Chavan AR, Singh AK, Purohit HJ, Khardenavis AA (2022) Role of heterotrophic nitrifiers and aerobic denitrifiers in simultaneous nitrification and denitrification process: a nonconventional nitrogen removal pathway in wastewater treatment. Lett Appl Microbiol 74:159–184

    Article  CAS  PubMed  Google Scholar 

  • Gupta RK, Singh AK, Bajaj A, Khardenavis AA, Purohit HJ (2023) Phylogenomic analysis of Citrobacter sp. strain AAK_AS5 and its metabolic capabilities to support nitrogen removal behaviour. J Basic Microbiol 63(3-4):359–376

    Article  PubMed  Google Scholar 

  • Helling RB (1998) Pathway choice in glutamate synthesis in Escherichia coli. J Bacteriol 180:4571–4575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang HK, Tseng SK (2001) Nitrate reduction by Citrobacter diversus under aerobic environment. Appl Microbiol Biotechnol 55:9–94

  • Hu Y, Zhao Y, Zhao X, Kumar JL (2012) High rate nitrogen removal in an alum sludge-based intermittent aeration constructed wetland. Environ Sci Technol 46:4583–4590

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Li W, Zhang D, Qin W (2013) Ammonium removal by a novel oligotrophic Acinetobacter sp. Y16 capable of heterotrophic nitrification–aerobic denitrification at low temperature. Bioresour Technol 146:44–50

    Article  CAS  Google Scholar 

  • Jeong BC, Hawes C, Bonthrone KM, Macaskie LE (1997) Localization of enzymically enhanced heavy metal accumulation by Citrobacter sp. and metal accumulation in vitro by liposomes containing entrapped enzyme. Microbiology 143:2497–2507

    Article  CAS  PubMed  Google Scholar 

  • Kalbar PP, Policy E (2021) Hybrid treatment systems: a paradigm shift to achieve sustainable wastewater treatment and recycling in India. Clean Technol Environ Policy 23:1365–1373

    Article  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3(3):109–136

    Article  CAS  PubMed  Google Scholar 

  • Khalid A, Arshad M, Crowley DE (2009) Biodegradation potential of pure and mixed bacterial cultures for removal of 4-nitroaniline from textile dye wastewater. Water Res 43:1110–1116

    Article  CAS  PubMed  Google Scholar 

  • Khardenavis AA, Kapley A, Purohit HJ (2007a) Simultaneous nitrification and denitrification by diverse Diaphorobacter sp. Appl Microbiol Biotechnol 77:403–409

    Article  CAS  PubMed  Google Scholar 

  • Khardenavis AA, Kumar MS, Mudliar SN, Chakrabarti T (2007b) Biotechnological conversion of agro-industrial wastewaters into biodegradable plastic, poly β-hydroxybutyrate. Bioresour Technol 98:3579–3584

    Article  CAS  PubMed  Google Scholar 

  • Khardenavis AA, Vaidya AN, Kumar MS, Chakrabarti T (2009) Utilization of molasses spentwash for production of bioplastics by waste activated sludge. Waste Manag 29:2558–2565

    Article  CAS  PubMed  Google Scholar 

  • Konstantinidis KT, Tiedje JMJ (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 102:2567–2572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuypers MM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263

    Article  CAS  PubMed  Google Scholar 

  • Langergraber G, Rieger L, Winkler S, Alex J, Wiese J, Owerdieck C, Maurer M (2004) A guideline for simulation studies of wastewater treatment plants. Water Sci Technol 50(7):131–138

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Ngo HH, Guo W, Peng L, Wang D, Ni B (2019) The roles of free ammonia (FA) in biological wastewater treatment processes: a review. Environ Int 123:10–19

    Article  CAS  PubMed  Google Scholar 

  • Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu YJG (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:2047-2217X-2041–2018

    Article  Google Scholar 

  • Luque I, Flores E, Herrero A (1994) Nitrate and nitrite transport in the cyanobacterium Synechococcus sp. PCC 7942 are mediated by the same permease. Biochim Biophys Acta (BBA)-Bioenerget 1184(2–3):296–298

    Article  CAS  Google Scholar 

  • Maier RM (2015) Chapter 16- biogeochemical cycling. In: Pepper IL, Gerba CP, Gentry TJ (eds) Environmental microbiology, 3rd edn. Academic Press, pp 339–373

  • Markande AR, Kapagunta C, Patil PS, Nayak BB (2016) Effective remediation of fish processing waste using mixed culture biofilms capable of simultaneous nitrification and denitrification. J Basic Microbiol 56(9):1046–1050

    Article  CAS  PubMed  Google Scholar 

  • McGinnis S, Madden TLJ (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:W20–W25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merchán F, Kindle KL, Llama MJ, Serra JL, Fernández E (1995) Cloning and sequencing of the nitrate transport system from the thermophilic, filamentous cyanobacterium Phormidium laminosum: comparative analysis with the homologous system from Synechococcus sp. PCC 7942. Plant Mol Biol 28(4):759–766

    Article  PubMed  Google Scholar 

  • Meti RS, Ambarish S, Khajure PV (2011) Enzymes of ammonia assimilation in fungi: an overview. Recent Res Sci Technol 2(4):28–38

  • Mhlanga FT, Foxon KM, Fennemore C, Mzulwini D, Buckley CA (2009) Simulation of a wastewater treatment plant receiving industrial effluents. Water SA 35(4):447–454

    Article  CAS  Google Scholar 

  • Moloantoa KM, Khetsha ZP, van Heerden E, Castillo JC, Cason ED (2022) Nitrate Water Contamination from Industrial Activities and Complete Denitrification as a Remediation Option. Water 14(5):799

    Article  CAS  Google Scholar 

  • Moreno-Vivián C, Cabello P, Martínez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181(21):6573–6584

    Article  PubMed  PubMed Central  Google Scholar 

  • Nájera AF, Serwecińska L, Mankiewicz-Boczek J (2021) Culturable nitrogen-transforming bacteria from sequential sedimentation biofiltration systems and their potential for nutrient removal in urban polluted rivers. Sci Rep 11:1–13

    Google Scholar 

  • Ogawa KI, Akagawa E, Yamane K, Sun ZW, LaCelle M, Zuber P, Nakano MM (1995) The nasB operon and nasA gene are required for nitrate/nitrite assimilation in Bacillus subtilis. J Bacteriol 177(5):1409–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Falush D, Keane JA, Parkhill J (2015) Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31:3691–3693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pal RR, Khardenavis AA, Purohit HJ (2015) Identification and monitoring of nitrification and denitrification genes in Klebsiella pneumoniae EGD-HP19-C for its ability to perform heterotrophic nitrification and aerobic denitrification. Funct Integr Genom 15:63–76

    Article  CAS  Google Scholar 

  • Pan M, Henry LG, Liu R, Huang X (2014) Nitrogen removal from slaughterhouse wastewater through partial nitrification followed by denitrification in intermittently aerated sequencing batch reactors at 11degree C. Environ Technol 35(1–4):470–477

    Article  CAS  PubMed  Google Scholar 

  • Pan Z, Zhou J, Lin Z, Wang Y, Zhao P, Zhou J, Liu S, He XJ (2020) Effects of COD/TN ratio on nitrogen removal efficiency, microbial community for high saline wastewater treatment based on heterotrophic nitrification-aerobic denitrification process. Bioresour Technol 301:122726

    Article  CAS  PubMed  Google Scholar 

  • Pandey D, Verma S, Verma P, Mahanty B, Dutta K, Daverey A, Arunachalam K (2021) SARS-CoV-2 in wastewater: challenges for developing countries. Int J Hygiene Environ Health 231:113634

    Article  CAS  Google Scholar 

  • Papaspyrou S, Smith CJ, Dong LF, Whitby C, Dumbrell AJ, Nedwell DB (2014) Nitrate reduction functional genes and nitrate reduction potentials persist in deeper estuarine sediments. Why? PLoS ONE 9:e94111

    Article  PubMed  PubMed Central  Google Scholar 

  • Paradis S, Boissinot M, Paquette N, Bélanger SD, Martel EA, Boudreau DK, Picard FJ, Ouellette M, Roy PH, Bergeron MG et al (2005) Phylogeny of the Enterobacteriaceae based on genes encoding elongation factor Tu and F-ATPase β-subunit. Int J Syst Evol Microbiol 55:2013–2025

    Article  CAS  PubMed  Google Scholar 

  • Rahimi S, Modin O, Mijakovic I (2020) Technologies for biological removal and recovery of nitrogen from wastewater. Biotechnol Adv 43:107570

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, Konstantinidis KT (2018) The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res 46:W282–W288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez‐R LM, Harvey WT, Rosselló‐Mora R, Tiedje JM, Cole JR, Konstantinidis KT (2020) Classifying prokaryotic genomes using the Microbial Genomes Atlas (MiGA) webserver. Bergey's Manual of Systematics of Archaea and Bacteria, pp 1–11

  • Shakya AK, Ghosh PK (2018) Simultaneous removal of arsenic, iron and nitrate in an attached growth bioreactor tomeet drinking water standards: Importance of sulphate and empty bed contact time. J Clean Prod 186:1011–1020

    Article  CAS  Google Scholar 

  • Shastry RP, Welch M, Rai VR, Ghate SD, Sandeep K, Rekha P (2020) The whole-genome sequence analysis of Enterobacter cloacae strain Ghats1: insights into endophytic lifestyle-associated genomic adaptations. Arch Microbiol 202:1571–1579

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, Gupta RK, Purohit HJ, Khardenavis AA (2022) Genomic characterization of denitrifying methylotrophic Pseudomonas aeruginosa strain AAK/M5 isolated from municipal solid waste landfill soil. World J Microbiol Biotechnol 38:140

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Zhang H, Cheng Z, Wang S (2017) Effect of low aeration rate on simultaneous nitrification and denitrification in an intermittent aeration aged refuse bioreactor treating leachate. Waste Manag 63:410–416

    Article  CAS  PubMed  Google Scholar 

  • Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11:472–477

    Article  CAS  PubMed  Google Scholar 

  • Tikariha H, Purohit HJ (2019) Assembling a genome for novel nitrogen-fixing bacteria with capabilities for utilization of aromatic hydrocarbons. Genomics 111:1824–1830

    Article  CAS  PubMed  Google Scholar 

  • Tilahun L, Asrat A, Wessel GM, Simachew A (2021) In silico determination of nitrogen metabolism in microbes from extreme conditions using metagenomics. Arch Microbiol 203:2521–2540

    Article  CAS  PubMed  Google Scholar 

  • Tiso M, Schechter AN (2015) Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions. PLoS ONE 10:e0119712

    Article  PubMed  PubMed Central  Google Scholar 

  • Tusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624

    Article  Google Scholar 

  • Vatsala T, Raj SM, Manimaran A (2008) A pilot-scale study of biohydrogen production from distillery effluent using defined bacterial co-culture. Int J Hydrogen Energy 33:5404–5415

    Article  CAS  Google Scholar 

  • Wang J-T, Chang S-C (2016) Citrobacter species. http://www.antimicrobe.org/b93.asp. Accessed 21 Dec 2021

  • Watanabe M, Kojima H, Fukui M (2017) Draft genome sequence of Desulfoplanes formicivorans Pf12B T, a sulfate-reducing bacterium of the family Desulfomicrobiaceae. Stand Genomic Sci 12:1–5

    Article  Google Scholar 

  • Wei Y, Ji M, Li R, Qin F (2012) Organic and nitrogen removal from landfill leachate in aerobic granular sludge sequencing batch reactors. Waste Manag 32(3):448–455

    Article  CAS  PubMed  Google Scholar 

  • Welsh A, Chee-Sanford JC, Connor LM, Löffler FE, Sanford RA (2014) Refined NrfA phylogeny improves PCR-based nrfA gene detection. Appl Environ Microbiol 80:2110–2119

    Article  PubMed  PubMed Central  Google Scholar 

  • Wen Y, Wei C-H (2011) Heterotrophic nitrification and aerobic denitrification bacterium isolated from anaerobic/anoxic/oxic treatment system. Afr J Biotech 10:6985–6990

    CAS  Google Scholar 

  • Wood NJ (2001) Nitrate and nitrite transport in bacteria. Cell Mol Life Sci CMLS 58(2):215–224

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Zhu Z, Fu L, Niu B, Li W (2011) WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genom 12:1–9

    Article  Google Scholar 

  • Xia L, Li X, Fan W, Wang JJBT (2020a) Heterotrophic nitrification and aerobic denitrification by a novel Acinetobacter sp. ND7 isolated from municipal activated sludge. Bioresour Technol 301:122749

    Article  CAS  PubMed  Google Scholar 

  • Xia Y, Zhang M, Tsang DC, Geng N, Lu D, Zhu L, Igalavithana AD, Dissanayake PD, Rinklebe J, Yang XJABC (2020b) Recent advances in control technologies for non-point source pollution with nitrogen and phosphorous from agricultural runoff: current practices and future prospects. Appl Biol Chem 63:1–13

    Article  Google Scholar 

  • Xu H, Wang X, Yu X, Zhang J, Guo L, Huang C, Jiang X, Li X, Feng Y, Zheng BJEp. (2018) First detection and genomics analysis of KPC-2-producing Citrobacter isolates from river sediments. Environ Pollut 235:931–937

    Article  CAS  PubMed  Google Scholar 

  • Yang X-P, Wang S-M, Zhang D-W, Zhou L-X (2011) Isolation and nitrogen removal characteristics of an aerobic heterotrophic nitrifying–denitrifying bacterium, Bacillus subtilis A1. Bioresour Technol 102:854–862

    Article  CAS  PubMed  Google Scholar 

  • Zala SL, Ayyer J, Desai AJ (2004) Nitrate removal from the effluent of a fertilizer industry using a bioreactor packed with immobilized cells of Pseudomonas stutzeri and Comamonas testosterone. World J Microbiol Biotechnol 20:661–665

    Article  CAS  Google Scholar 

  • Zhao T, Chen P, Zhang L, Zhang L, Gao Y, Ai S, Liu H, Liu XJBT (2021) Heterotrophic nitrification and aerobic denitrification by a novel Acinetobacter sp. TAC-1 at low temperature and high ammonia nitrogen. Bioresour Technol 339:125620

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Zhang P, Zhang J, Xu W, Wang X, Wu L, Sheng D, Ma W, Cao G, Xl C (2019) The developmental regulator MtrA binds GlnR boxes and represses nitrogen metabolism genes in Streptomyces coelicolor. Mol Microbiol 112:29–46

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge Director, CSIR-NEERI, and AcSIR-NEERI for providing essential resources for the research work. The manuscript has been checked for similarity by iThenticate software and has been assigned the manuscript number KRC No. CSIR-NEERI/KRC/2022/Jan/EBGD/1. RKG is thankful to University Grants Commission New Delhi, for the Senior Research Fellowship for carrying out this research.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

Authors

Contributions

RKG: Investigation, Formal analysis, Visualization, Data curation, Writing—Original draft. HT: Resources, Visualization, Data curation. HJP: Supervision, Methodology, Formal analysis, Writing—Review, and Editing. AAK: Writing—Review and Editing.

Corresponding author

Correspondence to Anshuman A. Khardenavis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Yusuf Akhter.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 448 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gupta, R.K., Tikariha, H., Purohit, H.J. et al. Pangenome-driven insights into nitrogen metabolic characteristics of Citrobacter portucalensis strain AAK_AS5 associated with wastewater nitrogen removal. Arch Microbiol 205, 270 (2023). https://doi.org/10.1007/s00203-023-03597-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-023-03597-7

Keywords

Navigation