Microbial responses to the use of NaClO in sediment treatment
Kun Li1,3, Tingming Ye1,3, Wang Zhang4, Jianfeng Peng2, Yaohui Bai1,3, Weixiao Qi2(), Huijuan Liu2
1. Key Laboratory of Drinking Water Science and Technology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China 2. Center for Water and Ecology, State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China 3. University of Chinese Academy of Sciences, Beijing 100049, China 4. China University of Mining & Technology, Beijing 100083, China
• Chlorine addition enhanced the release of TOC, TN from the sediment.
• Chlorine has a long-term negative effect on microbial richness.
• Usually enzymes lose activity, and expression of genes was downregulated.
• Carbon degradation and nitrification might be strongly inhibited.
Chlorine is often used in algal removal and deodorization of landscape waters, and occasionally used as an emergency treatment of heavily polluted sediments. However, the ecological impact of this practice has not been fully studied and recognized. In this study, NaClO at 0.1 mmol/g based on dry weight sediment was evenly mixed into the polluted sediment, and then the sediment was incubated for 150 days to evaluate its microbial effect. Results showed that NaClO addition enhanced the release of TOC, TN, Cr and Cu from the sediment. The microbial richness in the examined sediment decreased continuously, and the Chao1 index declined from 4241 to 2731, in 150 days. The microbial community composition was also changed. The abundance of Proteobacteria and Bacteroidetes increased to 54.8% and 4.2% within 7 days compared to the control, and linear discriminant analysis (LDA) showed gram-negative bacteria and aerobic bacteria enriched after chlorination. The functional prediction with PICRUSt2 showed the functions of the microbial community underwent major adjustments, and the metabolic-related functions such as carbon metabolism, including pyruvate and methane metabolisms were significantly inhibited; besides, 15 out of 22 analyzed key enzymes involved in C cycling and 6 out of 12 key enzymes or genes involved in N cycling were strongly impacted, and the enzymes and genes involved in carbon degradation and denitrification showed remarkable downregulation. It can be concluded that chlorination posed a seriously adverse effect on microbial community structure and function. This study deepens the understanding of the ecological effects of applying chlorine for environmental remediation.
. [J]. Frontiers of Environmental Science & Engineering, 2022, 16(2): 17.
Kun Li, Tingming Ye, Wang Zhang, Jianfeng Peng, Yaohui Bai, Weixiao Qi, Huijuan Liu. Microbial responses to the use of NaClO in sediment treatment. Front. Environ. Sci. Eng., 2022, 16(2): 17.
M Ahmad, A S Bajahlan, M M Miran (2011). Assessment of odour problem in sewage-treated effluent in a closed loop irrigation system. Environmental Monitoring and Assessment, 176(1–4): 31–42 https://doi.org/10.1007/s10661-010-1564-7
2
Apha (2012). Standard Methods for the Examination of Water and Wastewater. Washington, DC, USA: American Public Health Association
3
D L Ashley, M M Smith, L K Silva, Y M Yoo, B C De Jesús V R, Blount (2020). Factors associated with exposure to trihalomethanes, NHANES 2001–2012. Environmental Science & Technology, 54(2): 1066–1074 https://doi.org/10.1021/acs.est.9b05745
4
J Awad, J van Leeuwen, C Chow, M Drikas, R J Smernik, D J Chittleborough, Bestland E (2016). Characterization of dissolved organic matter for prediction of trihalomethane formation potential in surface and sub-surface waters. Journal of Hazardous Materials, 308: 430–439 https://doi.org/10.1016/j.jhazmat.2016.01.030
5
K Bagramyan, A Galstyan, A Trchounian (2000). Redox potential is a determinant in the Escherichia coli anaerobic fermentative growth and survival: effects of impermeable oxidant. Bioelectrochemistry (Amsterdam, Netherlands), 51(2): 151–156 https://doi.org/10.1016/S0302-4598(00)00065-9
6
Beier D, Gross R (2006). Regulation of bacterial virulence by two-component systems. Current Opinion in Microbiology, 9(2): 143–152 https://doi.org/10.1016/j.mib.2006.01.005
W M Brück, T B Brück, W T Self, J K Reed, S S Nitecki, P J McCarthy (2010). Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida. ISME Journal, 4(5): 686–699 https://doi.org/10.1038/ismej.2009.149
9
J X Cao, Q Sun, D H Zhao, M Y Xu, Q S Shen, D Wang, Y Wang, S M Ding (2020). A critical review of the appearance of black-odorous waterbodies in China and treatment methods. Journal of Hazardous Materials, 385(5): 121511 https://doi.org/10.1038/ismej.2009.149
S Choi, W Sim, D Jang, Y Yoon, J Ryu, J Oh, J S Woo, Y M Kim, Y Lee (2020). Antibiotics in coastal aquaculture waters: Occurrence and elimination efficiency in oxidative water treatment processes. Journal of Hazardous Materials, 396: 122585 https://doi.org/10.1016/j.jhazmat.2020.122585
12
J B da Costa, S Rodgher, L A Daniel, E L G Espíndola (2014). Toxicity on aquatic organisms exposed to secondary effluent disinfected with chlorine, peracetic acid, ozone and UV radiation. Ecotoxicology (London, England), 23(9): 1803–1813 https://doi.org/10.1007/s10646-014-1346-z
13
R Danovaro, P V R Snelgrove, P Tyler (2014). Challenging the paradigms of deep-sea ecology. Trends in Ecology & Evolution, 29(8): 465–475 https://doi.org/10.1016/j.tree.2014.06.002
14
J De Jonge M, P Teuchies, R Meire, L Blust, Bervoets (2012). The impact of increased oxygen conditions on metal-contaminated sediments part I: Effects on redox status, sediment geochemistry and metal bioavailability. Water Research, 46(7): 2205–2214 https://doi.org/10.1016/j.watres.2012.01.052
15
C M Dominguez, A Romero, A Checa-Fernandez, A Santos (2021). Remediation of HCHs-contaminated sediments by chemical oxidation treatments. Science of the Total Environment, 751: 141754 https://doi.org/10.1016/j.scitotenv.2020.141754
16
G M Douglas, V J Maffei, J R Zaneveld, S N Yurgel, J R Brown, C M Taylor, C Huttenhower, M G I Langille (2020). PICRUSt2 for prediction of metagenome functions. Nature Biotechnology, 38(6): 685–688 https://doi.org/10.1038/s41587-020-0548-6
17
V Ebenezer, Y V Nancharaiah, V P Venugopalan (2012). Chlorination-induced cellular damage and recovery in marine microalga, Chlorella salina. Chemosphere, 89(9): 1042–1047 https://doi.org/10.1016/j.chemosphere.2012.05.067
18
R C Edgar (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998 https://doi.org/10.1038/nmeth.2604
19
V Feigl, É Ujaczki, E Vaszita, M Molnár (2017). Influence of red mud on soil microbial communities: Application and comprehensive evaluation of the Biolog EcoPlate approach as a tool in soil microbiological studies. Science of the Total Environment, 595: 903–911 https://doi.org/10.1016/j.scitotenv.2017.03.266
20
E Ferrarese, G Andreottola, I A Oprea (2008). Remediation of PAH-contaminated sediments by chemical oxidation. Journal of Hazardous Materials, 152(1): 128–139 https://doi.org/10.1016/j.jhazmat.2007.06.080
21
M M Foley, J A Warrick, A Ritchie, A W Stevens, P B Shafroth, J J Duda, M M Beirne, R Paradis, G Gelfenbaum, R McCoy, E S Cubley (2017). Coastal habitat and biological community response to dam removal on the Elwha River. Ecological Monographs, 87(4): 552–577 https://doi.org/10.1002/ecm.1268
22
K E Furst, W A Pecson B M, Webber B D, Mitch (2018). Tradeoffs between pathogen inactivation and disinfection byproduct formation during sequential chlorine and chloramine disinfection for wastewater reuse. Water Research, 143: 579–588 https://doi.org/10.1016/j.watres.2018.05.050
23
A García-Ruiz M J, J Castellano-Hinojosa, F González-López, Osorio (2018). Effects of salinity on the nitrogen removal efficiency and bacterial community structure in fixed-bed biofilm CANON bioreactors. Chemical Engineering Journal, 347: 156–164 https://doi.org/10.1016/j.cej.2018.04.067
24
N Gu, Y X Wu, J L Gao, X Y Meng, P Zhao, H H Qin, K T Wang (2017). Microcystis aeruginosa removal by in situ chemical oxidation using persulfate activated by Fe2+ ions. Ecological Engineering, 99: 290–297 https://doi.org/10.1016/j.ecoleng.2016.11.048
25
A F Guerra, C Mellinger-Silva, A Rosenthal, R H Luchese (2018). Hot topic: Holder pasteurization of human milk affects some bioactive proteins. Journal of Dairy Science, 101(4): 2814–2818 https://doi.org/10.3168/jds.2017-13789
26
X M Han, Z W Wang, X Y Wang, X Zheng, J X Ma, Z C Wu (2016). Microbial responses to membrane cleaning using sodium hypochlorite in membrane bioreactors: Cell integrity, key enzymes and intracellular reactive oxygen species. Water Research, 88: 293–300 https://doi.org/10.1016/j.watres.2015.10.033
27
S Y Hu, T T Gong, Q M Xian, J J Wang, J Ma, Z G Li, J B Yin, B B Zhang, B Xu (2018). Formation of iodinated trihalomethanes and haloacetic acids from aromatic iodinated disinfection byproducts during chloramination. Water Research, 147: 254–263 https://doi.org/10.1016/j.watres.2018.09.058
28
Z Jiang, P Li, Y H Wang, B Li, Y X Wang (2013). Effects of roxarsone on the functional diversity of soil microbial community. International Biodeterioration & Biodegradation, 76: 32–35 https://doi.org/10.1016/j.ibiod.2012.06.010
29
S Jin, Y Sun, Z L Xu, Y M Bi, L F Sun (2014). Effects of residual chlorine discharged in water on the growth of phytoplankton. Acta Ecologica Sinica, 19: 5425–5433
30
B B Jørgensen, A Boetius (2007). Feast and famine- microbial life in the deep-sea bed. Nature Reviews. Microbiology, 5(10): 770–781 https://doi.org/10.1038/nrmicro1745
31
Kartal Ş, Aydın Z, Tokalıoğlu Ş (2006). Fractionation of metals in street sediment samples by using the BCR sequential extraction procedure and multivariate statistical elucidation of the data. Journal of Hazardous Materials, 132(1): 80–89 https://doi.org/10.1016/j.jhazmat.2005.11.091
32
J L Kelley, P F Grierson, S P Collin, P M Davies (2018). Habitat disruption and the identification and management of functional trait changes. Fish and Fisheries, 19(4): 716–728 https://doi.org/10.1111/faf.12284
33
V Krashevska, D Sandmann, M Maraun, S Scheu (2014). Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. ISME Journal, 8(5): 1126–1134 https://doi.org/10.1038/ismej.2013.209
34
H Kocour Kroupová, O Valentová, Z Svobodová, P Šauer, J Máchová (2018). Toxic effects of nitrite on freshwater organisms: a review. Reviews in Aquaculture, 10(3): 525–542 https://doi.org/10.1111/raq.12184
35
K Li, M Yang, J F Peng, R P Liu, T P Joshi, Y H Bai, H J Liu (2019). Rapid control of black and odorous substances from heavily-polluted sediment by oxidation: Efficiency and effects. Frontiers of Environmental Science & Engineering, 13(6): 87–97 https://doi.org/10.1007/s11783-019-1171-y
36
P Li, Z Jiang, Y H Wang, Y Deng, T Van Nostrand J D, H Yuan, D C Liu, J Z Wei, Zhou (2017). Analysis of the functional gene structure and metabolic potential of microbial community in high arsenic groundwater. Water Research, 123: 268–276 https://doi.org/10.1016/j.watres.2017.06.053
37
H H Liao, J Y Yen, Y J Guan, D F Ke, C X Liu (2020). Differential responses of stream water and bed sediment microbial communities to watershed degradation. Environment International, 134: 105198–105208 https://doi.org/10.1016/j.envint.2019.105198
T Z Liu, Z Zhang, Y Q Mao, D Y S Yan (2016). Induced metal redistribution and bioavailability enhancement in contaminated river sediment during in situ biogeochemical remediation. Environmental Science and Pollution Research International, 23(7): 6353–6362 https://doi.org/10.1007/s11356-015-5842-3
X Lu, C Fan, W He, J Deng, H Yin (2013). Sulfur-containing amino acid methionine as the precursor of volatile organic sulfur compounds in algea-induced black bloom. Journal of Environmental Sciences-China, 25(1): 33–43 https://doi.org/10.1016/S1001-0742(12)60019-9
42
X T Lv, X Zhang, Y Du, Q Y Wu, Y Lu, H Y Hu (2017). Solar light irradiation significantly reduced cytotoxicity and disinfection byproducts in chlorinated reclaimed water. Water Research, 125: 162–169 https://doi.org/10.1016/j.watres.2017.08.043
43
Y Lv, K K Xiao, J K Yang, Y W Zhu, K Y Pei, W B Yu, S Y Tao, H Wang, S Liang, H J Hou, B C Liu, J P Hu (2019). Correlation between oxidation-reduction potential values and sludge dewaterability during pre-oxidation. Water Research, 155(15): 96–105 https://doi.org/10.1016/j.watres.2019.02.049
M Nihemaiti, D A Le Roux J, J P Hoppe-Jones C, Reckhow, Croué (2017). Formation of haloacetonitriles, haloacetamides, and nitrogenous heterocyclic byproducts by chloramination of phenolic compounds. Environmental Science & Technology, 51(1): 655–663 https://doi.org/10.1021/acs.est.6b04819
46
M Premanathan, K Karthikeyan, K Jeyasubramanian, G Manivannan (2011). Selective toxicity of ZnO nanoparticles toward Gram-positive bacteria and cancer cells by apoptosis through lipid peroxidation. Nanomedicine (London), 7(2): 184–192 https://doi.org/10.1016/j.nano.2010.10.001
47
S Rajagopal, H A Van der Velde G, Van der Gaag M, Jenner (2003). How effective is intermittent chlorination to control adult mussel fouling in cooling water systems? Water Research, 37(2): 329–338 https://doi.org/10.1016/S0043-1354(02)00270-1
48
A R Ramos, A K G Tapia, C M N Piñol, N B Lantican, R D del Mundo M L F, M U Manalo, Herrera (2019). Morphological, electrical and antimicrobial properties of polyaniline-coated paper prepared via a two-pot layer-by-layer technique. Materials Chemistry and Physics, 238: 121972 https://doi.org/10.1016/j.matchemphys.2019.121972
49
V B Raquel, A E Manuel, B Erland, F C David (2019). Comparison of Cu salts and commercial Cu based fungicides on toxicity towards microorganisms in soil. Environmental Pollution, 257: 113585 https://doi.org/10.1016/j.envpol.2019.113585
50
H Sanawar, Y H Xiong, A Alam, J P Croué, P Y Hong (2017). Chlorination or monochloramination: Balancing the regulated trihalomethane formation and microbial inactivation in marine aquaculture waters. Aquaculture (Amsterdam, Netherlands), 480: 94–102 https://doi.org/10.1016/j.aquaculture.2017.08.014
51
I Sánchez-Andrea, I A Guedes, B Hornung, S Boeren, C E Lawson, D Z Sousa, A Bar-Even, N J Claassens, A J M Stams (2020). The reductive glycine pathway allows autotrophic growth of Desulfovibrio desulfuricans. Nature Communications, 11(1): 5090 https://doi.org/10.1038/s41467-020-18906-7
52
S R Schmidl, F Ekness, K Sofjan, K N Daeffler, K R Brink, B P Landry, K P Gerhardt, N Dyulgyarov, R U Sheth, J J Tabor (2019). Rewiring bacterial two-component systems by modular DNA-binding domain swapping. Nature Chemical Biology, 15(7): 690–698 https://doi.org/10.1038/s41589-019-0286-6
53
N Segata, J Izard, L Waldron, D Gevers, L Miropolsky, W S Garrett, C Huttenhower (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12(6): R60 https://doi.org/10.1186/gb-2011-12-6-r60
54
Q H Shen, J W Zhu, L H Cheng, J H Zhang, Z Zhang, X X Xu (2011). Enhanced algae removal by drinking water treatment of chlorination coupled with coagulation. Desalination, 271(1–3): 236–240 https://doi.org/10.1016/j.desal.2010.12.039
55
W C Shi, M C Li, G S Wei, R M Tian, C P Li, B Wang, R Lin, C Shi, X Chi, B Zhou, Z Gao (2019). The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome, 7(1): 14–31 https://doi.org/10.1186/s40168-019-0629-2
56
Y J Shih, N T Binh, C W Chen, C F Chen, C D Dong (2016). Treatability assessment of polycyclic aromatic hydrocarbons contaminated marine sediments using permanganate, persulfate and Fenton oxidation processes. Chemosphere, 150: 294–303 https://doi.org/10.1016/j.chemosphere.2016.01.112
57
B Song, M Chen, S J Ye, P Xu, G M Zeng, J L Gong, J Li, P Zhang, W C Cao (2019a). Effects of multi-walled carbon nanotubes on metabolic function of the microbial community in riverine sediment contaminated with phenanthrene. Carbon, 144: 1–7 https://doi.org/10.1016/j.carbon.2018.12.016
58
Y H Song, G N Mao, G H Gao, M Bartlam, Y Y Wang (2019b). Resistance and resilience of representative low nucleic acid-content bacteria to free chlorine exposure. Journal of Hazardous Materials, 365: 270–279 https://doi.org/10.1016/j.jhazmat.2018.10.080
59
E Soto, S Yun, W Surachetpong (2019). Susceptibility of Tilapia Lake Virus to buffered Povidone-iodine complex and chlorine. Aquaculture (Amsterdam, Netherlands), 512: 734342 https://doi.org/10.1016/j.aquaculture.2019.734342
60
F Suanon, Q Sun, B Dimon, D Mama, C P Yu (2016). Heavy metal removal from sludge with organic chelators: Comparative study of N, N-bis(carboxymethyl) glutamic acid and citric acid. Journal of Environmental Management, 166: 341–347 https://doi.org/10.1016/j.jenvman.2015.10.035
61
C Suquet, J J Warren, N Seth, J K Hurst (2010). Comparative study of HOCl-inflicted damage to bacterial DNA ex vivo and within cells. Archives of Biochemistry and Biophysics, 493(2): 135–142 https://doi.org/10.1016/j.abb.2009.10.006
62
A Tessier, P G C Campbell, M Bisson (1979). Sequential extraction procedure for the speciation of particular trace metals. Analytical Chemistry, 51(7): 844–851 https://doi.org/10.1021/ac50043a017
63
S Venkatnarayanan, P Sriyutha Murthy, Y V Nancharaiah, R Kirubagaran, V P Venugopalan (2017). Chlorination induced damage and recovery in marine diatoms: Assay by SYTOX® Green staining. Marine Pollution Bulletin, 124(2): 819–826 https://doi.org/10.1016/j.marpolbul.2016.12.059
64
J Wang, Z N Hao, F Q Shi, Y G Yin, D Cao, Z W Yao, J F Liu (2018). Characterization of brominated disinfection byproducts formed during the chlorination of aquaculture seawater. Environmental Science & Technology, 52(10): 5662–5670 https://doi.org/10.1021/acs.est.7b05331
65
L L Wang, X X Yuan, H Zhong, H Wang, Z B Wu, X H Chen, G Zeng (2014). Release behavior of heavy metals during treatment of dredged sediment by microwave-assisted hydrogen peroxide oxidation. Chemical Engineering Journal, 258: 334–340 https://doi.org/10.1016/j.cej.2014.07.098
66
Y H Wang, Y H Wu, X Tong, T Yu, L Peng, Y Bai, X H Zhao, Z Y Huo, N Ikuno, H Y Hu (2019). Chlorine disinfection significantly aggravated the biofouling of reverse osmosis membrane used for municipal wastewater reclamation. Water Research, 154: 246–257 https://doi.org/10.1016/j.watres.2019.02.008
67
N B Weston, S B Joye (2005). Temperature-driven decoupling of key phases of organic matter degradation in marine sediments. Proceedings of the National Academy of Sciences of the United States of America, 102(47): 17036–17040 https://doi.org/10.1073/pnas.0508798102
J Xiao, Q Y Liu, J H Du, W L Zhu, Q Y Li, X L Chen, X H Chen, H Liu, X Y Zhou, Y Z Zhao, H L Wang (2020). Integrated analysis of physiological, transcriptomic and metabolomic responses and tolerance mechanism of nitrite exposure in Litopenaeus vannamei. Science of the Total Environment, 711: 134416 https://doi.org/10.1016/j.scitotenv.2019.134416
70
M Y Xu, Q Zhang, C Y Xia, Y M Zhong, G P Sun, J Guo, T Yuan, J Z Zhou, Z L He (2014). Elevated nitrate enriches microbial functional genes for potential bioremediation of complexly contaminated sediments. ISME Journal, 8(9): 1932–1944 https://doi.org/10.1038/ismej.2014.42
71
C H Yang, P Yang, J Geng, H B Yin, K N Chen (2020). Sediment internal nutrient loading in the most polluted area of a shallow eutrophic lake (Lake Chaohu, China) and its contribution to lake eutrophication. Environmental Pollution, 262: 114292–114301 https://doi.org/10.1016/j.envpol.2020.114292
72
Z Yang, R P Buley, E G Fernandez-Figueroa, M U G Barros, S Rajendran, A E Wilson (2018). Hydrogen peroxide treatment promotes chlorophytes over toxic cyanobacteria in a hyper-eutrophic aquaculture pond. Environmental Pollution, 240: 590–598 https://doi.org/10.1016/j.envpol.2018.05.012
73
Y Y Ye, P H Chang, J Hartert, K R Wigginton (2018). Reactivity of enveloped virus genome, proteins, and lipids with free chlorine and UV254. Environmental Science & Technology, 52(14): 7698–7708 https://doi.org/10.1021/acs.est.8b00824
74
X Yin, J H Li, H D Shin, G C Du, L Liu, J Chen (2015). Metabolic engineering in the biotechnological production of organic acids in the tricarboxylic acid cycle of microorganisms: Advances and prospects. Biotechnology Advances, 33(6): 830–841 https://doi.org/10.1016/j.biotechadv.2015.04.006
Y Zhu, W H Fan, T T Zhou, X M Li (2019). Removal of chelated heavy metals from aqueous solution: A review of current methods and mechanisms. Science of the Total Environment, 678: 253–266 https://doi.org/10.1016/j.scitotenv.2019.04.416
