Abstract
Dealing with nitrogen-rich saline wastewater produced by industries remains challenging because of the inhibition of functional microorganisms by high salinity. The underlying mechanisms of anaerobic ammonium-oxidizing bacteria (AnAOB) exposed to salinity stress should be studied to investigate the potential of anaerobic ammonium oxidation (ANAMMOX) for applications in such wastewater. In this study, the total DNA from granular sludge was extracted from an expanded granular sludge bed (EGSB) reactor operated at 0, 15 and 30 g/L salinity and subjected to high-throughput sequencing. The nitrogen removal performance in the reactor could be maintained from 86.2 to 88.0% at less than 30 g/L salinity level. The microbial diversity in the reactor under saline conditions was lower than that under the salt-free condition. Three genera of AnAOB were detected in the reactor, and Candidatus Kuenenia was the most abundant. The predictive functional profiling based on the Clusters of Orthologous Groups of proteins (COGs) database showed that the inhibition of AnAOB under saline conditions was mainly characterised by the weakening of energy metabolism and intracellular repair. AnAOB might adapt to salinity stress by increasing their rigidity and intracellular osmotic pressure. The predictive functional profiling based on the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database revealed that the inhibition of AnAOB was mainly manifested by the weakening of intracellular carbohydrate and lipid metabolism, the blockage of intracellular energy supply and the reduction of membrane transport capacity. AnAOB might adapt to salinity stress by strengthening wall/membrane synthesis, essential cofactors (porphyrins) and energy productivity, enhancing intracellular material transformation and gene repair and changing its structure and group behaviour. The stability of the nitrogen removal performance could be maintained via the adaptation of AnAOB to salinity and their increased abundance.
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References
Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York
APHA, AWWA, WEF (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC
Cao S, Du R, Li B, Ren N, Peng Y (2016) High-throughput profiling of microbial community structures in an ANAMMOX–UASB reactor treating high-strength wastewater. Appl Microbiol Biot 100:6457–6467. https://doi.org/10.1007/s00253-016-7427-6
Da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Biotechnology of extremophiles. Springer, New York, pp 117–153
Dapena-Mora A, Campos J, Mosquera-Corral A, Méndez R (2006) Anammox process for nitrogen removal from anaerobically digested fish canning effluents. Water Sci Technol 53:265–274. https://doi.org/10.2166/wst.2006.429
Diepold A, Armitage JP (2015) Type III secretion systems: the bacterial flagellum and the injectisome. Philos Trans R Soc Lond B Biol Sci 370:20150020. https://doi.org/10.1098/rstb.2015.0020
Epstein W (2003) The roles and regulation of potassium in bacteria. Prog Nucleic Acid Res Mol Biol 75:293–320. https://doi.org/10.1016/S0079-6603(03)75008-9
Fan X-Y, Gao J-F, Pan K-L, Li D-C, Dai H-H (2017) Temporal dynamics of bacterial communities and predicted nitrogen metabolism genes in a full-scale wastewater treatment plant. RSC Adv 7:56317–56327. https://doi.org/10.1039/c7ra10704h
Fang F, Yang M-M, Wang H, Yan P, Chen Y-P, Guo J-S (2018) Effect of high salinity in wastewater on surface properties of anammox granular sludge. Chemosphere 210:366–375. https://doi.org/10.1016/j.chemosphere.2018.07.038
Field A (2013) Discovering statistics using IBM SPSS statistics. Sage, New York
Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. https://doi.org/10.1126/science.1124234
Giustinianovich EA, Campos J-L, Roeckel MD, Estrada AJ, Mosquera-Corral A, del Río ÁV (2018) Influence of biomass acclimation on the performance of a partial nitritation-anammox reactor treating industrial saline effluents. Chemosphere 194:131–138. https://doi.org/10.1016/j.chemosphere.2017.11.146
Gonzalez-Silva BM, Rønning AJ, Andreassen IK, Bakke I, Cervantes FJ, Østgaard K, Vadstein O (2017) Changes in the microbial community of an anammox consortium during adaptation to marine conditions revealed by 454 pyrosequencing. Appl Microbiol Biot 101:5149–5162. https://doi.org/10.1007/s00253-017-8160-5
Green ER, Mecsas J (2016) Bacterial secretion systems—an overview. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.VMBF-0012-2015
Henderson JF, Paterson ARP (2014) Nucleotide metabolism: an introduction. Academic, Cambridge
Jacobs K, Lebel L, Buizer J, Addams L, Matson P, McCullough E, Garden P, Saliba G, Finan T (2016) Linking knowledge with action in the pursuit of sustainable water-resources management. Proc Natl Acad Sci USA 113:4591–4596. https://doi.org/10.1073/pnas.0813125107
Jin R-C, Ma C, Mahmood Q, Yang G-F, Zheng P (2011) Anammox in a UASB reactor treating saline wastewater. Process Saf Environ Prot 89:342–348. https://doi.org/10.1016/j.psep.2011.05.001
Jin R-C, Yang G-F, Yu J-J, Zheng P (2012) The inhibition of the Anammox process: a review. Chem Eng J 197:67–79. https://doi.org/10.1016/j.cej.2012.05.014
Kartal B, de Almeida NM, Maalcke WJ, Op den Camp HJ, Jetten MS, Keltjens JT (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37:428–461. https://doi.org/10.1111/1574-6976.12014
Kartal B, Koleva M, Arsov R, van der Star W, Jetten MS, Strous M (2006) Adaptation of a freshwater anammox population to high salinity wastewater. J Biotechnol 126:546–553. https://doi.org/10.1016/j.jbiotec.2006.05.012
Kartal B, Kuenen JV, Van Loosdrecht M (2010) Sewage treatment with anammox. Science 328:702–703. https://doi.org/10.1126/science.1185941
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814. https://doi.org/10.1038/nbt.2676
Lewinson O, Livnat-Levanon N (2017) Mechanism of action of ABC importers: conservation, divergence, and physiological adaptations. J Mol Biol 429:606–619. https://doi.org/10.1016/j.jmb.2017.01.010
Li Z-X, Zhang L, Chen X-B, Li H, Li D (2015) Acclimation of a highly-efficient and seawater tolerant anammox sludge. J Environ Sci (China) 35:748–756
Liu C, Yamamoto T, Nishiyama T, Fujii T, Furukawa K (2009) Effect of salt concentration in anammox treatment using non woven biomass carrier. J Biosci Bioeng 107:519–523. https://doi.org/10.1016/j.jbiosc.2009.01.020
Ma C, Jin R-C, Yang G-F, Yu J-J, Xing B-S, Zhang Q-Q (2012) Impacts of transient salinity shock loads on Anammox process performance. Bioresour Technol 112:124–130. https://doi.org/10.1016/j.biortech.2012.02.122
Meng Y, Yin C, Zhou Z, Meng F (2018) Increased salinity triggers significant changes in the functional proteins of ANAMMOX bacteria within a biofilm community. Chemosphere 207:655–664. https://doi.org/10.1016/j.chemosphere.2018.05.076
Nelson DL, Cox MM (2008) Glycolysis, gluconeogenesis, and the pentose phosphate pathway. Lehninger principles of biochemistry, 4th edn. W.H. Freeman, New York, pp 521–559
Paredes D, Kuschk P, Mbwette T, Stange F, Müller R, Köser H (2007) New aspects of microbial nitrogen transformations in the context of wastewater treatment—a review. Eng Life Sci 7:13–25. https://doi.org/10.1002/elsc.200620170
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Qiao S, Bi Z, Zhou J, Cheng Y, Zhang J (2013) Long term effects of divalent ferrous ion on the activity of anammox biomass. Bioresour Technol 142:490–497. https://doi.org/10.1016/j.biortech.2013.05.062
Rønning AJ (2013) Adaptation of anaerobic ammonium oxidizing (anammox) bacteria to salinity in a continuous reactor. MS thesis. Institutt for bioteknologi
Sheetz MP, Sable JE, Döbereiner H-G (2006) Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu Rev Biophys Biomol Struct 35:417–434. https://doi.org/10.1146/annurev.biophys.35.040405.102017
Shinohara T, Qiao S, Yamamoto T, Nishiyama T, Fujii T, Kaiho T, Bhatti Z, Furukawa K (2009) Partial nitritation treatment of underground brine waste with high ammonium and salt content. J Biosci Bioeng 108:330–335. https://doi.org/10.1016/j.jbiosc.2009.04.014
Speth DR, Lagkouvardos I, Wang Y, Qian P-Y, Dutilh BE, Jetten MS (2017) Draft genome of Scalindua rubra, obtained from the interface above the discovery deep brine in the Red Sea, sheds light on potential salt adaptation strategies in anammox bacteria. Microb Ecol 74:1–5. https://doi.org/10.1007/s00248-017-0929-7
Tang C-J, Zheng P, Mahmood Q, Chen J-W (2009) Start-up and inhibition analysis of the Anammox process seeded with anaerobic granular sludge. J Ind Microbiol Biotechnol 36:1093. https://doi.org/10.1007/s10295-009-0593-0
Uygur A (2006) Specific nutrient removal rates in saline wastewater treatment using sequencing batch reactor. Process Biochem 41:61–66. https://doi.org/10.1016/j.procbio.2005.03.068
Van de Graaf AA, de Bruijn P, Robertson LA, Jetten MS, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiol 142:2187–2196. https://doi.org/10.1099/13500872-142-8-2187
Van de Graaf AA, Mulder A, de Bruijn P, Jetten M, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61:1246–1251
Van Der Star WR, Miclea AI, Van Dongen UG, Muyzer G, Picioreanu C, Van Loosdrecht MC (2008) The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 101:286–294. https://doi.org/10.1002/bit.21891
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. https://doi.org/10.1038/ncomms7878
Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544
Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024. https://doi.org/10.1038/nrm1524
Wang K, Ye X, Zhang H, Chen H, Zhang D, Liu L (2016) Regional variations in the diversity and predicted metabolic potential of benthic prokaryotes in coastal northern Zhejiang, East China Sea. Sci Rep 6:38709. https://doi.org/10.1038/srep38709
Wei Q, Kawagoshi Y, Huang X, Hong N, Van Duc L, Yamashita Y, Hama T (2016) Nitrogen removal properties in a continuous marine anammox bacteria reactor under rapid and extensive salinity changes. Chemosphere 148:444–451. https://doi.org/10.1016/j.chemosphere.2016.01.041
Xie W, Wang F, Guo L, Chen Z, Sievert SM, Meng J, Huang G, Li Y, Yan Q, Wu S (2011) Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. ISME J 5:414. https://doi.org/10.1038/ismej.2010.144
Xing H, Wang H, Fang F, Li K, Liu L, Chen Y, Guo J (2017) Effect of increase in salinity on ANAMMOX–UASB reactor stability. Environ Technol 38:1184–1190. https://doi.org/10.1080/09593330.2016.1223174
Yang J, Zhang L, Hira D, Fukuzaki Y, Furukawa K (2011) Anammox treatment of high-salinity wastewater at ambient temperature. Bioresour Technol 102:2367–2372. https://doi.org/10.1016/j.biortech.2010.10.101
Zhang Z-Z, Ji Y-X, Cheng Y-F, Jin R-C (2018) Increased salinity improves the thermotolerance of mesophilic anammox consortia. Sci Total Environ 644:710–716. https://doi.org/10.1016/j.scitotenv.2018.07.027
Zhou E, Trepat X, Park C, Lenormand G, Oliver M, Mijailovich S, Hardin C, Weitz D, Butler J, Fredberg J (2009) Universal behavior of the osmotically compressed cell and its analogy to the colloidal glass transition. Proc Natl Acad Sci USA 106:10632–10637. https://doi.org/10.1073/pnas.0901462106
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This study was funded by the National Natural Science Foundation of China (Grant nos. 51878091 and 21876016).
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Wang, H., Li, HX., Fang, F. et al. Underlying mechanisms of ANAMMOX bacteria adaptation to salinity stress. J Ind Microbiol Biotechnol 46, 573–585 (2019). https://doi.org/10.1007/s10295-019-02137-x
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DOI: https://doi.org/10.1007/s10295-019-02137-x