Bioaerosolization behavior along sewage sludge biostabilization
Fan Lu1,2, Tianyu Hu1,2, Shunyan Wei1,2, Liming Shao3, Pinjing He1,2,3()
1. State Key Laboratory of Pollution Control and Source Reuse, Tongji University, Shanghai 200092, China 2. Shanghai Institute of Pollution Control and Ecological Security, Shanghai 200092, China 3. Institute of Waste Treatment and Reclamation, Tongji University, Shanghai 200092, China
• Aerosolization behavior during a lab-scale sludge biostabilization was determined.
• Many pathogenic species were identified to be preferentially aerosolized.
• Bioaerosol concentration along the biostabilization ranged from 160 to 1440 cell/m3.
• Sludge aerosolization behavior was different with that of other biowaste.
Biostabilization is a cost-effective method for the beneficial utilization of sewage sludge. However, during the operation of sludge biostabilization, some microbial species could be released into the atmospheric environment from the solid-phase of sludge easily and present a high risk to human health. This study aimed to evaluate the risk of bioaerosol during sludge biostabilization. We found a total of nine bacterial phyla, one archaeal phylum, and two fungal phyla in the bioaerosol samples. Among them, Proteobacteria, Actinobacteria, Bacteroidetes, and Ascomycota were the dominant phyla. In addition, the bioaerosolization indexes (BI) of prokaryotic phyla and fungal phyla ranged 0–45 and 0–487, respectively. Massilia, Pseudarthrobacter, Pseudomonas, Tremellales spp., and Fusarium were the preferentially aerosolized microbial genera with maximum bioaerosolization indexes of 19962, 10360, 1802, 3055, and 7398. The bioaerosol concentration during the biostabilization ranged from 160 to 1440 cell/m3, and we identified species such as Stenotrophomonas rhizophila and Fusarium graminerum with high bioaerosolization indexes that could be threats to human health. Euryachaeota, which belongs to archaeal phyla, had the highest biostabilization index in our study. We also found that Pseudarthrobacter was the easiest to aerosolize during the sludge biostabilization process.
E G Abbasian, M Bayat, A C Nosrati, S J Hashemi, M Ghoranneviss (2020). The effect of atmospheric plasma jet on Fusarium species producing mycotoxins T2 and DON: An approach for physical and chemical investigation. Eurasian Chemical Communication, 2(3): 340–348 https://doi.org/10.33945/SAMI/ECC.2020.3.5
2
S Amir, G Merlina, E Pinelli, P Winterton, J C Revel, M Hafidi (2008). Microbial community dynamics during composting of sewage sludge and straw studied through phospholipid and neutral lipid analysis. Journal of Hazardous Materials, 159(2–3): 593–601 https://doi.org/10.1016/j.jhazmat.2008.02.062
3
M K Awasthi, Z Zhang, Q Wang, F Shen, R Li, D S Li, X Ren, M Wang, H Chen, J Zhao (2017). New insight with the effects of biochar amendment on bacterial diversity as indicators of biomarkers support the thermophilic phase during sewage sludge composting. Bioresource Technology, 238: 589–601 https://doi.org/10.1016/j.biortech.2017.04.100
4
C Barrera, P Wild, V Dorribo, D Savova-Bianchi, A Laboissiere, J A Pralong, B Danuser, P Krief, L Millon, G Reboux, H Niculita-Hirzel (2018). Exposure to field vs. storage wheat dust: different consequences on respiratory symptoms and immune response among grain workers. International Archives of Occupational and Environmental Health, 91(6): 745–757 https://doi.org/10.1007/s00420-018-1322-7
5
B Breza-Boruta, Z Paluszak (2009). Emission of bioaerosol from a mechanical biological sewage treatment plant. Przemysl Chemiczny, 88(5): 402–405
6
J S Brooke (2012). Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clinical Microbiology Reviews, 25(1): 2–41 https://doi.org/10.1128/CMR.00019-11
7
V R Cahyani, A Watanabe, K Matsuya, S Asakawa, M Kimura (2002). Succession of microbiota estimated by phospholipid fatty acid analysis and changes in organic constituents during the composting process of rice straw. Soil Science and Plant Nutrition, 48(5): 735–743 https://doi.org/10.1080/00380768.2002.10409264
8
Y C Chung (2007). Evaluation of gas removal and bacterial community diversity in a biofilter developed to treat composting exhaust gases. Journal of Hazardous Materials, 144(1–2): 377–385 https://doi.org/10.1016/j.jhazmat.2006.10.045
9
R R Da Silva, R Pedezzi, T B Souto (2017). Exploring the bioprospecting and biotechnological potential of white-rot and anaerobic Neocallimastigomycota fungi: peptidases, esterases, and lignocellulolytic enzymes. Applied Microbiology and Biotechnology, 101(8): 3089–3101 https://doi.org/10.1007/s00253-017-8225-5
10
V De Gannes, G Eudoxie, W J Hickey (2013). Prokaryotic successions and diversity in composts as revealed by 454-pyrosequencing. Bioresource Technology, 133: 573–580 https://doi.org/10.1016/j.biortech.2013.01.138
11
P De Giudici, M T Guillam, C Segala, G Keck (2013). Microbiological risk assessment of waste management activities: composting and sewage sludge application. Environnement Risques & Sante, 12(5): 422–433
12
Y Ding, J Xiong, B Zhou, J Wei, A Qian, H Zhang, W Zhu, J Zhu (2019). Odor removal by and microbial community in the enhanced landfill cover materials containing biochar-added sludge compost under different operating parameters. Waste Management (New York, N.Y.), 87: 679–690 https://doi.org/10.1016/j.wasman.2019.03.009
13
P Feeney, S F Rodríguez, R Molina, E Mcgillicuddy, S Hellebust, M Quirke, S Daly, D O’connor, J Sodeau (2018). A comparison of on-line and off-line bioaerosol measurements at a biowaste site. Waste Management (New York, N.Y.), 76: 323–338 https://doi.org/10.1016/j.wasman.2018.02.035
14
L Gauthier-Levesque, L Bonifait, N Turgeon, M Veillette, P Perrott, D Grenier, C Duchaine (2016). Impact of serotype and sequence type on the preferential aerosolization of Streptococcus suis. BMC Research Notes, 9(1): 273 https://doi.org/10.1186/s13104-016-2073-8
R J Gruninger, A K Puniya, T M Callaghan, J E Edwards, N Youssef, S S Dagar, K Fliegerova, G W Griffith, R Forster, A Tsang, T Mcallister, M S Elshahed (2014). Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential. FEMS Microbiology Ecology, 90(1): 1–17 https://doi.org/10.1111/1574-6941.12383
17
H Gu, Y Chen, X Liu, H Wang, J Shen-Tu, L Wu, L Zeng, J Xu (2017a). The effective migration of Massilia sp WF1 by Phanerochaete chrysosporium and its phenanthrene biodegradation in soil. Science of the Total Environment, 593–594: 695–703 https://doi.org/10.1016/j.scitotenv.2017.03.205
18
W Gu, Y Lu, Z Tan, P Xu, K Xie, X Li, L Sun (2017b). Fungi diversity from different depths and times in chicken manure waste static aerobic composting. Bioresource Technology, 239: 447–453 https://doi.org/10.1016/j.biortech.2017.04.047
19
Y Guo, E R Rene, J Wang, W Ma (2020). Biodegradation of polyaromatic hydrocarbons and the influence of environmental factors during the co-composting of sewage sludge and green forest waste. Bioresource Technology, 297: 122434 https://doi.org/10.1016/j.biortech.2019.122434
20
Y Han, T Yang, T Chen, L Li, J Liu (2019). Characteristics of submicron aerosols produced during aeration in wastewater treatment. Science of the Total Environment, 696: 134019 https://doi.org/10.1016/j.scitotenv.2019.134019
21
P He, W Du, X Xu, H Zhang, L Shao, F Lu (2020). Effect of biochemical composition on odor emission potential of biowaste during aerobic biodegradation. Science of the Total Environment, 727: 138285 https://doi.org/10.1016/j.scitotenv.2020.138285
22
P He, S Wei, L Shao, F Lu (2019). Aerosolization behavior of prokaryotes and fungi during composting of vegetable waste. Waste Management (New York, N.Y.), 89: 103–113 https://doi.org/10.1016/j.wasman.2019.04.008
23
J Jiang, Y Wang, J Liu, X Yang, Y Ren, H Miao, Y Pan, J Lv, G Yan, L Ding, Y Li (2019). Exploring the mechanisms of organic matter degradation and methane emission during sewage sludge composting with added vesuvianite: Insights into the prediction of microbial metabolic function and enzymatic activity. Bioresource Technology, 286: 121397 https://doi.org/10.1016/j.biortech.2019.121397
24
I H Kim, K Y Kim, C G Phae, D K Kim(2020). Effect of mechanical agitation on generation of airborne bacteria and endotoxin in exhaust gases from lab-scale composting of sewage sludge. Journal of Korean Society of Environmental Engineers, 34(3): 143–148 https://doi.org/10.4491/KSEE.2012.34.3.143
25
S Kohlmeier, T H M Smits, R M Ford, C Keel, H Harms, L Y Wick (2005). Taking the fungal highway: Mobilization of pollutant-degrading bacteria by fungi. Environmental Science & Technology, 39(12): 4640–4646 https://doi.org/10.1021/es047979z
26
W Lainhart (2018). Fusarium spp., a genus of common plant pathogens that can cause devastating, opportunistic human disease. Clinical Microbiology Newsletter, 40(1): 1–5 https://doi.org/10.1016/j.clinmicnews.2017.12.001
27
A Langarica-Fuentes, U Zafar, A Heyworth, T Brown, G Fox, G D Robson (2014). Fungal succession in an in-vessel composting system characterized using 454 pyrosequencing. FEMS Microbiology Ecology, 88(2): 296–308 https://doi.org/10.1111/1574-6941.12293
28
C Li, H Li, T Yao, M Su, F Ran, B Han, J Li, X Lan, Y Zhang, X Yang, S Gun (2019). Microbial inoculation influences bacterial community succession and physicochemical characteristics during pig manure composting with corn straw. Bioresource Technology, 289: 121653 https://doi.org/10.1016/j.biortech.2019.121653
29
Y Li, Y Liu, X Yong, X Wu, H Jia, J W C Wong, H Wu, J Zhou (2020). Odor emission and microbial community succession during biogas residue composting covered with a molecular membrane. Bioresource Technology, 297: 122518 https://doi.org/10.1016/j.biortech.2019.122518
30
D Lindquist, D Murrill, W P Burran, G Winans, J M Janda, W Probert (2003). Characteristics of Massilia timonae and Massilia timonae-like isolates from human patients, with an emended description of the species. Journal of Clinical Microbiology, 41(1): 192–196 https://doi.org/10.1128/JCM.41.1.192-196.2003
31
M Liu, M K Nobu, J Ren, X Jin, G Hong, H Yao (2020a). Bacterial compositions in inhalable particulate matters from indoor and outdoor wastewater treatment processes. Journal of Hazardous Materials, 385: 121515 https://doi.org/10.1016/j.jhazmat.2019.121515
32
T Liu, S K Awasthi, Y Duan, Z Zhang, M K Awasthi (2020b). Effect of fine coal gasification slag on improvement of bacterial diversity community during the pig manure composting. Bioresource Technology, 304: 123024 https://doi.org/10.1016/j.biortech.2020.123024
33
F Lu, L M Shao, H Zhang, W D Fu, S J Feng, L T Zhan, Y M Chen, P J He (2018). Application of advanced techniques for the assessment of bio-stability of biowaste-derived residues: A minireview. Bioresource Technology, 248: 122–133 https://doi.org/10.1016/j.biortech.2017.06.045
34
P Madamarandawala, Y Weerasinghe, D Pathiraja, A Ekanayake, D Madegedara, D Magana-Arachchi (2019). Impact of microbial air quality in preschools on paediatric respiratory health. Sn Applied Sciences, 1(10): 1280 https://doi.org/10.1007/s42452-019-1306-6
35
H Mbareche, M Veillette, L Bonifait, M E Dubuis, Y Benard, G Marchand, G J Bilodeau, C Duchaine (2017). A next generation sequencing approach with a suitable bioinformatics workflow to study fungal diversity in bioaerosols released from two different types of composting plants. Science of the Total Environment, 601– 602: 1306–1314 https://doi.org/10.1016/j.scitotenv.2017.05.235
36
J M Michaud, L R Thompson, D Kaul, J L Espinoza, R A Richter, Z Z Xu, C Lee, K M Pham, C M Beall, F Malfatti, F Azam, R Knight, M D Burkart, C L Dupont, K A Prather (2018). Taxon-specific aerosolization of bacteria and viruses in an experimental ocean-atmosphere mesocosm. Nature Communications, 9(1): 2017 https://doi.org/10.1038/s41467-018-04409-z
37
M Moletta, J P Delgenes, J J Godon (2007). Differences in the aerosolization behavior of microorganisms as revealed through their transport by biogas. Science of the Total Environment, 379(1): 75–88 https://doi.org/10.1016/j.scitotenv.2007.02.019
38
M Moletta-Denat, V Bru-Adan, J P Delgenes, J Hamelin, N Wery, J J Godon (2010). Selective microbial aerosolization in biogas demonstrated by quantitative PCR. Bioresource Technology, 101(19): 7252–7257 https://doi.org/10.1016/j.biortech.2010.04.035
39
H Niculita-Hirzel, G Hantier, F Storti, G Plateel, T Roger (2016). Frequent occupational exposure to Fusarium mycotoxins of workers in the swiss grain industry. Toxins, 8(12): 370 https://doi.org/10.3390/toxins8120370
40
OSHA(Occupational Safety and Health Administration) (1994). “Indoor air quality-proposed rule” notice of proposed rulemaking. Federal Register, 59(65): 15968–16039
41
A K Pahari, D Dasgupta, R S Patil, S Mukherji (2016). Emission of bacterial bioaerosols from a composting facility in Maharashtra, India. Waste Management (New York, N.Y.), 53: 22–31 https://doi.org/10.1016/j.wasman.2016.04.027
42
L J Pankhurst, C Whitby, M Pawlett, L D Larcombe, B Mckew, L J Deacon, S L Morgan, R Villa, G H Drew, S Tyrrel, S J T Pollard, F Coulon (2012). Temporal and spatial changes in the microbial bioaerosol communities in green-waste composting. FEMS Microbiology Ecology, 79(1): 229–239 https://doi.org/10.1111/j.1574-6941.2011.01210.x
43
B C Parker, M A Ford, H Gruft, J O Falkinham (1983). Epidemiology of infection by nontuberculous mycobacteria: IV. Preferential aerosolization of Mycobacterium-intracellulare from natural-waters. American Review of Respiratory Disease, 128(4): 652–656
44
J Peng, K Wang, X Yin, X Yin, M Du, Y Gao, P Antwi, N Ren, A Wang (2019). Trophic mode and organics metabolic characteristic of fungal community in swine manure composting. Frontiers of Environmental Science & Engineering, 13(6): 137–146 https://doi.org/10.1007/s11783-019-1177-5
45
P Perrott, N Turgeon, L Gauthier-Levesque, C Duchaine (2017). Preferential aerosolization of bacteria in bioaerosols generated invitro. Journal of Applied Microbiology, 123(3): 688–697 https://doi.org/10.1111/jam.13514
46
S Ravva, C Sarreal, R Mandrell (2011). Bacterial communities in aerosols and manure samples from two different dairies in central and sonoma valleys of california. PLoS One, 6(2): e17281 https://doi.org/10.1371/journal.pone.0017281
47
S Robertson, P Douglas, D Jarvis, E Marczylo (2019). Bioaerosol exposure from composting facilities and health outcomes in workers and in the community: A systematic review update. International Journal of Hygiene and Environmental Health, 222(3): 364–386 https://doi.org/10.1016/j.ijheh.2019.02.006
48
C Robledo-Mahón, Gomez-Silvan, G L Andersen, C Calvo, E Aranda (2020). Assessment of bacterial and fungal communities in a full-scale thermophilic sewage sludge composting pile under a semipermeable cover. Bioresource Technology, 298: 122550 https://doi.org/10.1016/j.biortech.2019.122550
49
T Robledo-Mahón, M A Martin, M C Gutierrez, M Toledo, I Gonzalez, E Aranda, A F Chica, C Calvo (2019). Sewage sludge composting under semi-permeable film at full-scale: evaluation of odour emissions and relationships between microbiological activities and physico-chemical variables. Environmental Research, 177: 108624 https://doi.org/10.1016/j.envres.2019.108624
50
M Rodriguez-Diaz, F Cerrone, M Sanchez-Peinado, L Santacruz-Calvo, C Pozo, J G López (2014). Massilia umbonata sp: nov., able to accumulate poly-beta-hydroxybutyrate, isolated from a sewage sludge compost-soil microcosm. International Journal of Systematic and Evolutionary Microbiology, 64(Pt_1): 131–137 https://doi.org/10.1099/ijs.0.049874-0
V Shestivska, K Dryahina, J Nunvar, K Sovova, D Elhottova, A Nemec, D Smith, P Spanel (2015). Quantitative analysis of volatile metabolites released in vitro by bacteria of the genus Stenotrophomonas for identification of breath biomarkers of respiratory infection in cystic fibrosis. Journal of Breath Research, 9(2): 027104 https://doi.org/10.1088/1752-7155/9/2/027104
53
D J Springer, D Saini, E J Byrnes, J Heitman, R Frothingham (2013). Development of an aerosol model of Cryptococcus reveals humidity as an important factor affecting the viability of Cryptococcus during aerosolization. PLoS One, 8(7): e69804 https://doi.org/10.1371/journal.pone.0069804
54
K Steger, A M Sjögren , A Jarvis, J K Jansson, I Sundh (2007). Development of compost maturity and Actinobacteria populations during full-scale composting of organic household waste. Journal of Applied Microbiology, 103(2): 487–498 https://doi.org/10.1111/j.1365-2672.2006.03271.x
55
J Q Su, B Wei, W Y Ou-Yang, F Y Huang, Y Zhao, H J Xu, Y G Zhu (2015). Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environmental Science & Technology, 49(12): 7356–7363 https://doi.org/10.1021/acs.est.5b01012
56
Z Tang, B Xi, C Huang, W Tan, W Li, X Zhao, K Liu, X Xia (2020). Mobile genetic elements in potential host microorganisms are the key hindrance for the removal of antibiotic resistance genes in industrial-scale composting with municipal solid waste. Bioresource Technology, 301: 122723 https://doi.org/10.1016/j.biortech.2019.122723
57
M Veillette, L Bonifait, H Mbareche, G Marchand, C Duchaine (2018). Preferential aerosolization of Actinobacteria during handling of composting organic matter. Journal of Aerosol Science, 116: 83–91 https://doi.org/10.1016/j.jaerosci.2017.11.004
58
J Vinzelj, A Joshi, H Insam, S M Podmirseg (2020). Employing anaerobic fungi in biogas production: Challenges & opportunities. Bioresource Technology, 300: 122687 https://doi.org/10.1016/j.biortech.2019.122687
59
J Wang, Z Liu, J Xia, Y Chen (2019). Effect of microbial inoculation on physicochemical properties and bacterial community structure of citrus peel composting. Bioresource Technology, 291: 121843 https://doi.org/10.1016/j.biortech.2019.121843
60
Y Wang, L Liu, J Yang, Y Duan, Y Luo, M J Taherzadeh, Y Li, H Li, M K Awasthi, Z Zhao (2020). The diversity of microbial community and function varied in response to different agricultural residues composting. Science of the Total Environment, 715: 136983 https://doi.org/10.1016/j.scitotenv.2020.136983
61
M Wei, C Xu, X Xu, C Zhu, J Li, G Lv (2019). Characteristics of atmospheric bacterial and fungal communities in PM2.5 following biomass burning disturbance in a rural area of North China Plain. Science of the Total Environment, 651: 2727–2739 https://doi.org/10.1016/j.scitotenv.2018.09.399
62
Y Wei, Y Zhao, H Wang, Q Lu, Z Cao, H Cui, L Zhu, Z Wei (2016). An optimized regulating method for composting phosphorus fractions transformation based on biochar addition and phosphate-solubilizing bacteria inoculation. Bioresource Technology, 221: 139–146 https://doi.org/10.1016/j.biortech.2016.09.038
63
L Y Wick, R Remer, B Würz , J Reichenbach, S Braun, F Schäfer , H Harms (2007). Effect of fungal hyphae on the access of bacteria to phenanthrene in soil. Environmental Science & Technology, 41(2): 500–505 https://doi.org/10.1021/es061407s
64
Y Yang, H Yin, H Peng, G Lu, Z Dang (2020). Biodegradation of triphenyl phosphate using an efficient bacterial consortium GYY: Degradation characteristics, metabolic pathway and 16S rRNA genes analysis. Science of the Total Environment, 713: 136598 https://doi.org/10.1016/j.scitotenv.2020.136598
65
H Zhang, H Sun, R Yang, S Li, M Zhou, T Gao, L An, X Chen, P Dyson (2016a). Complete genome sequence of a psychotrophic Pseudarthrobacter sulfonivorans strain Ar51 (CGMCC 4.7316), a novel crude oil and multi benzene compounds degradation strain. Journal of Biotechnology, 231: 81–82 https://doi.org/10.1016/j.jbiotec.2016.04.010
66
L Zhang, Y Jia, X Zhang, X Feng, J Wu, L Wang, G Chen (2016b). Wheat straw: an inefficient substrate for rapid natural lignocellulosic composting. Bioresource Technology, 209: 402–406 https://doi.org/10.1016/j.biortech.2016.03.004
67
X Zhao, Y Wei, F Zhang, W Tan, Y Fan, B Xi (2019). How do fungal communities and their interaction with bacterial communities influence dissolved organic matter on the stability and safety of sludge compost? Environmental Science and Pollution Research International, 26(4): 4141–4146 https://doi.org/10.1007/s11356-018-4023-6
68
G Zhou, X Xu, X Qiu, J Zhang (2019). Biochar influences the succession of microbial communities and the metabolic functions during rice straw composting with pig manure. Bioresource Technology, 272: 10–18 https://doi.org/10.1016/j.biortech.2018.09.135
69
H B Zhou, C Ma, D Gao, T B Chen, G D Zheng, J Chen, T H Pan (2014). Application of a recyclable plastic bulking agent for sewage sludge composting. Bioresource Technology, 152: 329–336 https://doi.org/10.1016/j.biortech.2013.10.061
70
R Zittel, C P Da Silva, C E Domingues, D C H Seremeta, K M Da Cunha, S X De Campos (2020). Availability of nutrients, removal of nicotine, heavy metals and pathogens in compounds obtained from smuggled cigarette tobacco compost associated with industrial sewage sludge. Science of the Total Environment, 699: 134377 https://doi.org/10.1016/j.scitotenv.2019.134377