Microbial Ecology

, Volume 78, Issue 2, pp 428–445 | Cite as

Structural and Functional Changes of Groundwater Bacterial Community During Temperature and pH Disturbances

  • Yuhao Song
  • Guannan Mao
  • Guanghai Gao
  • Mark BartlamEmail author
  • Yingying WangEmail author
Environmental Microbiology


In this study, we report the characteristics of a microbial community in sampled groundwater and elucidate the effects of temperature and pH disturbances on bacterial structure and nitrogen-cycling functions. The predominant phyla of candidate OD1, candidate OP3, and Proteobacteria represented more than half of the total bacteria, which clearly manifested as a “low nucleic acid content (LNA) bacteria majority” type via flow cytometric fingerprint. The results showed that LNA bacteria were more tolerant to rapid changes in temperature and pH, compared to high nucleic acid content (HNA) bacteria. A continuous temperature increase test demonstrated that the LNA bacterial group was less competitive than the HNA bacterial group in terms of maintaining their cell intactness and growth potential. In contrast, the percentage of intact LNA bacteria was maintained at nearly 70% with pH decrease, despite a 50% decrease in total intact cells. Next-generation sequencing results revealed strong resistance and growth potential of phylum Proteobacteria when the temperature increased or the pH decreased in groundwater, especially for subclasses α-, β-, and γ-Proteobacteria. In addition, relative abundance of nitrogen-related functional genes by qPCR showed no difference in nitrifiers or denitrifiers within 0.45 μm-captured and 0.45 μm-filterable bacteria due to phylogenetic diversity. One exception was the monophyletic anammox bacteria that belong to the phylum Planctomycetes, which were mostly captured on a 0.45-μm filter. Furthermore, we showed that both temperature increase and pH decrease could enhance the denitrification potential, whereas the nitrification and anammox potentials were weakened.


Groundwater Microbial community structure Filtration Nitrogen-cycling functional genes Flow cytometry 



This study was funded by the National Natural Science Foundation of China (No.31670498 and 31322012).

Supplementary material

248_2019_1333_MOESM1_ESM.docx (357 kb)
ESM 1 (DOCX 357 kb)


  1. 1.
    Braun B, Schroder J, Knecht H, Szewzyk U (2016) Unraveling the microbial community of a cold groundwater catchment system. Water Res 107:113–126. CrossRefPubMedGoogle Scholar
  2. 2.
    Besmer MD, Epting J, Page RM, Sigrist JA, Huggenberger P, Hammes F (2016) Online flow cytometry reveals microbial dynamics influenced by concurrent natural and operational events in groundwater used for drinking water treatment. Sci Rep 6:38462. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Tufenkji N, Ryan JN, Elimelech M (2002) The promise of bank filtration. Environ Sci Technol36: 422AGoogle Scholar
  4. 4.
    Griebler C, Lueders T (2010) Microbial biodiversity in groundwater ecosystems. Freshw Biol 54:649–677 CrossRefGoogle Scholar
  5. 5.
    Bouvier T, Del Giorgio PA, Gasol JM (2007) A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environ Microbiol 9:2050–2066.
  6. 6.
    Wang Y, Hammes F, Boon N, Chami M, Egli T (2009) Isolation and characterization of low nucleic acid (LNA)-content bacteria. ISME J 3:889–902. CrossRefPubMedGoogle Scholar
  7. 7.
    Luef B, Frischkorn KR, Wrighton KC, Holman HY, Birarda G, Thomas BC, Singh A, Williams KH, Siegerist CE, Tringe SG, Downing KH, Comolli LR, Banfield JF (2015) Diverse uncultivated ultra-small bacterial cells in groundwater. Nat Commun 6:6372. CrossRefPubMedGoogle Scholar
  8. 8.
    Wang Y, Hammes F, Düggelin M, Egli T (2008) Influence of size, shape, and flexibility on bacterial passage through micropore membrane filters. Environ Sci Technol 42:6749–6754. CrossRefPubMedGoogle Scholar
  9. 9.
    Miteva VI, Brenchley JE (2005) Detection and isolation of ultrasmall microorganisms from a 120,000-year-old Greenland glacier ice core. Appl Environ Microbiol 71:7806–7818. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Proctor CR, Besmer MD, Langenegger T, Beck K, Walser JC, Ackermann M, Burgmann H, Hammes F (2018) Phylogenetic clustering of small low nucleic acid-content bacteria across diverse freshwater ecosystems. ISME J 12:1344–1359. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Ramseier MK, von Gunten U, Freihofer P, Hammes F (2011) Kinetics of membrane damage to high (HNA) and low (LNA) nucleic acid bacterial clusters in drinking water by ozone, chlorine, chlorine dioxide, monochloramine, ferrate (VI), and permanganate. Water Res 45:1490–1500. CrossRefPubMedGoogle Scholar
  12. 12.
    Laidlaw PP, Elford WJ (1936) A new group of filterable organisms. P Roy Soc B-Biol Sci 120:292–303CrossRefGoogle Scholar
  13. 13.
    Huete-Stauffer TM, Arandia-Gorostidi N, Alonso-Saez L, Moran XA (2016) Experimental warming decreases the average size and nucleic acid content of marine bacterial communities. Front Microbiol 7:730. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Hessen DO, Daufresne M, Leinaas HP (2013) Temperature-size relations from the cellular-genomic perspective. Biol Rev Camb Philos Soc 88:476–489. CrossRefPubMedGoogle Scholar
  15. 15.
    Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Chang 1:401–406. CrossRefGoogle Scholar
  16. 16.
    Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. PNAS 106:12788–12793. CrossRefPubMedGoogle Scholar
  17. 17.
    Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291. CrossRefPubMedGoogle Scholar
  18. 18.
    White EP, Ernest SK, Kerkhoff AJ, Enquist BJ (2007) Relationships between body size and abundance in ecology. Trends Ecol Evol 22:323–330. CrossRefPubMedGoogle Scholar
  19. 19.
    Sabath N, Ferrada E, Barve A, Wagner A (2013) Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol Evol 5:966–977. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. P Roy Soc B-Biol Sci 272:2561–2569. CrossRefGoogle Scholar
  21. 21.
    Meron D, Atias E, Iasur Kruh L, Elifantz H, Minz D, Fine M, Banin E (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5:51–60. CrossRefPubMedGoogle Scholar
  22. 22.
    Yanagawa K, Morono Y, de Beer D, Haeckel M, Sunamura M, Futagami T, Hoshino T, Terada T, Nakamura K, Urabe T, Rehder G, Boetius A, Inagaki F (2013) Metabolically active microbial communities in marine sediment under high-CO(2) and low-pH extremes. ISME J 7:555–567. CrossRefPubMedGoogle Scholar
  23. 23.
    Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811–1811. CrossRefPubMedGoogle Scholar
  24. 24.
    Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob Chang Biol 16:851–863. CrossRefGoogle Scholar
  25. 25.
    Vega TR, Willnerhall D, Rodriguezmueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163. CrossRefGoogle Scholar
  26. 26.
    Liu F, Sun J, Wang J, Zhang Y (2017) Groundwater acidification in shallow aquifers in Pearl River Delta, China: distribution, factors, and effects. Geochem J 51:373–384. CrossRefGoogle Scholar
  27. 27.
    Highton MP, Roosa S, Crawshaw J, Schallenberg M, Morales SE (2016) Physical factors correlate to microbial community structure and nitrogen cycling gene abundance in a nitrate fed eutrophic lagoon. Front Microbiol 7:1691. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. PNAS 96:5995–6000CrossRefGoogle Scholar
  29. 29.
    Hu Y, He F, Ma L, Zhang Y, Wu Z (2016) Microbial nitrogen removal pathways in integrated vertical-flow constructed wetland systems. Bioresour Technol 207:339–345. CrossRefPubMedGoogle Scholar
  30. 30.
    Zeng J, Lou K, Zhang CJ, Wang JT, Hu HW, Shen JP, Zhang LM, Han LL, Zhang T, Lin Q, Chalk PM, He JZ (2016) Primary succession of nitrogen cycling microbial communities along the deglaciated forelands of Tianshan Mountain, China. Front Microbiol 7:1353. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hammes F, Egli T (2005) New method for assimilable organic carbon determination using flow-cytometric enumeration and a natural microbial consortium as inoculum. Environ Sci Technol 39:3289–3294. CrossRefPubMedGoogle Scholar
  32. 32.
    Liu X, Wang J, Liu T, Kong W, He X, Jin Y, Zhang B (2015) Effects of assimilable organic carbon and free chlorine on bacterial growth in drinking water. PLoS One 10: e0128825Google Scholar
  33. 33.
    Vital M, Hammes F, Egli T (2012) Competition of Escherichia coli O157 with a drinking water bacterial community at low nutrient concentrations. Water Res 46:6279–6290. CrossRefPubMedGoogle Scholar
  34. 34.
    Berney M, Vital M, Hülshoff I, Weilenmann HU, Egli T, Hammes F (2008) Rapid, cultivation-independent assessment of microbial viability in drinking water. Water Res 42:4010–4018. CrossRefPubMedGoogle Scholar
  35. 35.
    Hammes F, Goldschmidt F, Vital M, Wang Y, Egli T (2010) Measurement and interpretation of microbial adenosine tri-phosphate (ATP) in aquatic environments. Water Res 44:3915–3923. CrossRefPubMedGoogle Scholar
  36. 36.
    Liu J, Hua ZS, Chen LX, Kuang JL, Li SJ, Shu WS, Huang LN (2014) Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous environment of mine tailings. Appl Environ Microbiol 80:3677–3686. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. CrossRefPubMedGoogle Scholar
  39. 39.
    Tsushima I, Kindaichi T, Okabe S (2007) Quantification of anaerobic ammonium-oxidizing bacteria in enrichment cultures by real-time PCR. Water Res 41:785–794. CrossRefPubMedGoogle Scholar
  40. 40.
    Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712PubMedPubMedCentralGoogle Scholar
  41. 41.
    Attard E, Poly F, Commeaux C, Laurent F, Terada A, Smets BF, Recous S, Roux XL (2010) Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environ Microbiol 12:315–326. CrossRefPubMedGoogle Scholar
  42. 42.
    Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Philippot L (2005) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 61:289–290. CrossRefGoogle Scholar
  43. 43.
    Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962. CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Hartman AL, Lough DM, Barupal DK, Fiehn O, Fishbein T, Zasloff M, Eisen JA, Gordon JI (2009) Human gut microbiome adopts an alternative state following small bowel transplantation. PNAS 106:17187–17192. CrossRefPubMedGoogle Scholar
  46. 46.
    Wang Y, Hammes F, Boon N, Egli T (2007) Quantification of the filterability of freshwater bacteria through 0.45, 0.22, and 0.1 m pore size filters and shape-dependent enrichment of filterable bacterial communities. Environ Sci Technol 41:7080–7086. CrossRefPubMedGoogle Scholar
  47. 47.
    Morita RY (1997) Bacteria in oligotrophic environments: starvation-survival lifestyle. Chapman & Hall, New York, pp 50–89Google Scholar
  48. 48.
    Kantor RS, Wrighton KC, Handley KM, Sharon I, Hug LA, Castelle CJ, Thomas BC, Banfield JF (2013) Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla. Mbio 4:00708–00713. CrossRefGoogle Scholar
  49. 49.
    Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503. CrossRefGoogle Scholar
  50. 50.
    Hahn MW (2004) Broad diversity of viable bacteria in ‘sterile’ (0.2 microm) filtered water. Res Microbiol 155:688–691. CrossRefPubMedGoogle Scholar
  51. 51.
    Haller CM, Rölleke S, Vybiral D, Witte A, Velimirov B (2000) Investigation of 0.2 μm filterable bacteria from the Western Mediterranean Sea using a molecular approach: dominance of potential starvation forms. FEMS Microbiol Ecol 31:153–161. CrossRefPubMedGoogle Scholar
  52. 52.
    Vybiral D, Denner EBM, Haller CM, Busse HJ, Witte A, Höfle MG, Velimirov B (1999) Polyphasic classification of 0.2 μm filterable bacteria from the Western Mediterranean Sea. Syst Appl Microbiol 22:635–646. CrossRefPubMedGoogle Scholar
  53. 53.
    Nimbkar N, Rajvanshi AK (2013) Simple filtration and low-temperature sterilization of drinking water. Curr Sci 104:519–522Google Scholar
  54. 54.
    Spinks AT, Dunstan RH, Harrison T, Coombes P, Kuczera G (2006) Thermal inactivation of water-borne pathogenic and indicator bacteria at sub-boiling temperatures. Water Res 40:1326–1332. CrossRefPubMedGoogle Scholar
  55. 55.
    Ciochetti DA, Metcalf RH (1984) Pasteurization of naturally contaminated water with solar energy. Appl Environ Microbiol 47:223–228PubMedPubMedCentralGoogle Scholar
  56. 56.
    Reineke K, Mathys A, Heinz V, Knorr D (2013) Mechanisms of endospore inactivation under high pressure. Trends Microbiol 21:296–304. CrossRefPubMedGoogle Scholar
  57. 57.
    Aüllo T, Ranchoupeyruse A, Ollivier B, Magot M (2013) Desulfotomaculum spp. and related gram-positive sulfate-reducing bacteria in deep subsurface environments. Front Microbiol 4: 362.
  58. 58.
    Hassani M, Mañas P, Raso J, Condón S, Pagán R (2005) Predicting heat inactivation of listeria monocytogenes under nonisothermal treatments. J Food Prot 68:736–743. CrossRefPubMedGoogle Scholar
  59. 59.
    Kim KT, Murano EA, Olson DG (2010) Heating and storage conditions affect survival and recovery of listeria monocytogenes in ground pork. J Food Sci 59:30–32. CrossRefGoogle Scholar
  60. 60.
    Eydal HS, Pedersen K (2007) Use of an ATP assay to determine viable microbial biomass in Fennoscandian Shield groundwater from depths of 3-1000 m. J Microbiol Methods 70:363–373. CrossRefPubMedGoogle Scholar
  61. 61.
    Nescerecka A, Juhna T, Hammes F (2016) Behavior and stability of adenosine triphosphate (ATP) during chlorine disinfection. Water Res 101:490–497. CrossRefPubMedGoogle Scholar
  62. 62.
    Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49. CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Najar IN, Sherpa MT, Das S, Das S, Thakur N (2018) Microbial ecology of two hot springs of Sikkim: predominate population and geochemistry. Sci Total Environ 637-638:730–745. CrossRefPubMedGoogle Scholar
  64. 64.
    Keshri J, Pradeep Ram AS, Nana PA, Sime-Ngando T (2018) Taxonomical resolution and distribution of bacterioplankton along the vertical gradient reveals pronounced spatiotemporal patterns in contrasted temperate freshwater lakes. Microb Ecol 76:372–386. CrossRefPubMedGoogle Scholar
  65. 65.
    Ghosh A, Bhadury P (2018). Exploring biogeographic patterns of bacterioplankton communities across global estuaries. Microbiologyopen:e741.
  66. 66.
    Jin D, Kong X, Cui B, Jin S, Xie Y, Wang X, Deng Y (2018) Bacterial communities and potential waterborne pathogens within the typical urban surface waters. Sci Rep 8:13368. CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Salmaso N, Albanese D, Capelli C, Boscaini A, Pindo M, Donati C (2018) Diversity and cyclical seasonal transitions in the bacterial community in a large and deep perialpine lake. Microb Ecol 76:125–143. CrossRefPubMedGoogle Scholar
  68. 68.
    Amin A, Ahmed I, Salam N, Kim BY, Singh D, Zhi XY, Xiao M, Li WJ (2017) Diversity and distribution of thermophilic bacteria in hot springs of Pakistan. Microb Ecol 74:1–12. CrossRefGoogle Scholar
  69. 69.
    López-López O, Knapik K, Cerdán ME, González-Siso MI (2015) Metagenomics of an alkaline hot spring in Galicia (Spain): microbial diversity analysis and screening for novel lipolytic enzymes. Front Microbiol 6.
  70. 70.
    Liu K, Liu Y, Jiao N, Xu B, Gu Z, Xing T, Xiong J (2017) Bacterial community composition and diversity in Kalakuli, an alpine glacial-fed lake in Muztagh Ata of the westernmost Tibetan Plateau. FEMS Microbiol Ecol 93: fix085.
  71. 71.
    Lew S, Glińska-Lewczuk K, Ziembińska-Buczyńska A (2018) Prokaryotic community composition affected by seasonal changes in physicochemical properties of water in peat bog lakes. Water 10:485. CrossRefGoogle Scholar
  72. 72.
    Longnecker K, Sherr BF, Sherr EB (2005) Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem. Appl Environ Microbiol 71:7737–7749. CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Read DS, Gweon HS, Bowes MJ, Newbold LK, Field D, Bailey MJ, Griffiths RI (2015) Catchment-scale biogeography of riverine bacterioplankton. ISME J 9:516–526. CrossRefPubMedGoogle Scholar
  74. 74.
    Padan E, Bibi E, Ito M, Krulwich TA (2005) Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta 1717:67–88. CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Padan E, Zilberstein D, Rottenberg H (1976) The proton electrochemical gradient in Escherichia coli cells. Eur J Biochem 63:533–541. CrossRefPubMedGoogle Scholar
  76. 76.
    Slonczewski JL, Rosen BP, Alger JR, Macnab RM (1981) pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. PNAS 78:6271–6275CrossRefGoogle Scholar
  77. 77.
    Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49:359–378PubMedPubMedCentralGoogle Scholar
  78. 78.
    Baatout S, Leys N, Hendrickx L, Dams A, Mergeay M (2007) Physiological changes induced in bacteria following pH stress as a model for space research. Acta Astronaut 60:451–459. CrossRefGoogle Scholar
  79. 79.
    Albert LS, Brown DG (2015) Variation in bacterial ATP concentration during rapid changes in extracellular pH and implications for the activity of attached bacteria. Colloid Surface B 132: 111.
  80. 80.
    Grinius L, Slusnyte R, Griniuviene B (1975) ATP synthesis driven by protonmotive force imposed across Escherichia coli cell membranes. FEBS Lett 57:290–293. CrossRefPubMedGoogle Scholar
  81. 81.
    Singh AP, Bragg PD (1979) ATP synthesis driven by a pH gradient imposed across the cell membranes of lipoic acid and unsaturated fatty acid auxotrophs of Escherichia coli. FEBS Lett 98:21–24. CrossRefPubMedGoogle Scholar
  82. 82.
    Nelson WC, Stegen JC (2015) The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle. Front Microbiol 6:713. CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Mclean JS, Lombardo MJ, Badger JH, Edlund A, Novotny M, Yee-Greenbaum J, Vyahhi N, Hall AP, Yang Y, Dupont CL (2013) Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. PNAS 110:2390–2399CrossRefGoogle Scholar
  84. 84.
    Ward L, Taylor MW, Power JF, Scott BJ, Mcdonald IR, Stott MB (2017) Microbial community dynamics in Inferno Crater Lake, a thermally fluctuating geothermal spring. ISME J 11:1158–1167. CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Shade A, Chiu CY, Mcmahon KD (2010) Differential bacterial dynamics promote emergent community robustness to lake mixing: an epilimnion to hypolimnion transplant experiment. Environ Microbiol 12:455–466. CrossRefPubMedGoogle Scholar
  86. 86.
    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239. CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Lindstrom ES, Kamst-Van Agterveld MP, Zwart G (2005) Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol 71:8201–8206. CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Wang H, Ji G, Bai X (2015) Enhanced long-term ammonium removal and its ranked contribution of microbial genes associated with nitrogen cycling in a lab-scale multimedia biofilter. Bioresour Technol 196:57–64. CrossRefPubMedGoogle Scholar
  89. 89.
    Wang L, Li T (2011) Anaerobic ammonium oxidation in constructed wetlands with bio-contact oxidation as pretreatment. Ecol Eng 37:1225–1230. CrossRefGoogle Scholar
  90. 90.
    Zhang L, Narita Y, Gao L, Ali M, Oshiki M, Ishii S, Okabe S (2017) Microbial competition among anammox bacteria in nitrite-limited bioreactors. Water Res 125:249–258. CrossRefPubMedGoogle Scholar
  91. 91.
    van Teeseling MC, Mesman RJ, Kuru E, Espaillat A, Cava F, Brun YV, Vannieuwenhze MS, Kartal B, van Niftrik L (2015) Anammox Planctomycetes have a peptidoglycan cell wall. Nat Commun 6:6878. CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Godde M, Conrad R (1999) Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification ad denitrification in two soils. Biol Fertil Soils 30:33–40. CrossRefGoogle Scholar
  93. 93.
    Holtan-Hartwig L, Dörsch P, Bakken LR (2002) Low temperature control of soil denitrifying communities: kinetics of N2O production and reduction. Soil Biol Biochem 34:1797–1806. CrossRefGoogle Scholar
  94. 94.
    Zhang L, Zeng G, Zhang J, Chen Y, Yu M, Lu L, Li H, Zhu Y, Yuan Y, Huang A (2015) Response of denitrifying genes coding for nitrite (nirK or nirS) and nitrous oxide (nosZ) reductases to different physico-chemical parameters during agricultural waste composting. Appl Microbiol Biotechnol 99:4059–4070. CrossRefPubMedGoogle Scholar
  95. 95.
    Deiglmayr K, Philippot L, Hartwig UA, Kandeler E (2004) Structure and activity of the nitrate-reducing community in the rhizosphere of Lolium perenne and Trifolium repens under long-term elevated atmospheric pCO2. FEMS Microbiol Ecol 49:445–454. CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of Education), Tianjin Key Laboratory of Environmental Remediation and Pollution Control, College of Environmental Science and EngineeringNankai UniversityTianjinChina
  2. 2.College of Life SciencesNankai UniversityTianjinChina

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