Bioaerosolization behavior along sewage sludge biostabilization
Fan Lu, Tianyu Hu, Shunyan Wei, Liming Shao, Pinjing He
Bioaerosolization behavior along sewage sludge biostabilization
• 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.
Sludge / Composting / Bioaerosol / Bioaerosolization index / High-throughput sequencing / 4′, 6-diamidino-2-phenylindole (DAPI)
[1] |
Abbasian E G, Bayat M, Nosrati A C, Hashemi S J, Ghoranneviss M (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
CrossRef
Google scholar
|
[2] |
Amir S, Merlina G, Pinelli E, Winterton P, Revel J C, Hafidi M (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
CrossRef
Google scholar
|
[3] |
Awasthi M K, Zhang Z, Wang Q, Shen F, Li R, Li D S, Ren X, Wang M, Chen H, Zhao J (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
CrossRef
Google scholar
|
[4] |
Barrera C, Wild P, Dorribo V, Savova-Bianchi D, Laboissiere A, Pralong J A, Danuser B, Krief P, Millon L, Reboux G, Niculita-Hirzel H (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
CrossRef
Google scholar
|
[5] |
Breza-Boruta B, Paluszak Z (2009). Emission of bioaerosol from a mechanical biological sewage treatment plant. Przemysl Chemiczny, 88(5): 402–405
|
[6] |
Brooke J S (2012). Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clinical Microbiology Reviews, 25(1): 2–41
CrossRef
Google scholar
|
[7] |
Cahyani V R, Watanabe A, Matsuya K, Asakawa S, Kimura M (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
CrossRef
Google scholar
|
[8] |
Chung Y C (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
CrossRef
Google scholar
|
[9] |
Da Silva R R, Pedezzi R, Souto T B (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
CrossRef
Google scholar
|
[10] |
De Gannes V, Eudoxie G, Hickey W J (2013). Prokaryotic successions and diversity in composts as revealed by 454-pyrosequencing. Bioresource Technology, 133: 573–580
CrossRef
Google scholar
|
[11] |
De Giudici P, Guillam M T, Segala C, Keck G (2013). Microbiological risk assessment of waste management activities: composting and sewage sludge application. Environnement Risques & Sante, 12(5): 422–433
|
[12] |
Ding Y, Xiong J, Zhou B, Wei J, Qian A, Zhang H, Zhu W, Zhu J (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
CrossRef
Google scholar
|
[13] |
Feeney P, Rodríguez S F, Molina R, Mcgillicuddy E, Hellebust S, Quirke M, Daly S, O’connor D, Sodeau J (2018). A comparison of on-line and off-line bioaerosol measurements at a biowaste site. Waste Management (New York, N.Y.), 76: 323–338
CrossRef
Google scholar
|
[14] |
Gauthier-Levesque L, Bonifait L, Turgeon N, Veillette M, Perrott P, Grenier D, Duchaine C (2016). Impact of serotype and sequence type on the preferential aerosolization of Streptococcus suis. BMC Research Notes, 9(1): 273
CrossRef
Google scholar
|
[15] |
Glass N L, Schmoll M, Cate J H D, Coradetti S (2013). Plant cell wall deconstruction by Ascomycete fungi. Annual Review of Microbiology, 67(1): 477–498
CrossRef
Google scholar
|
[16] |
Gruninger R J, Puniya A K, Callaghan T M, Edwards J E, Youssef N, Dagar S S, Fliegerova K, Griffith G W, Forster R, Tsang A, Mcallister T, Elshahed M S (2014). Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential. FEMS Microbiology Ecology, 90(1): 1–17
CrossRef
Google scholar
|
[17] |
Gu H, Chen Y, Liu X, Wang H, Shen-Tu J, Wu L, Zeng L, Xu J (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
CrossRef
Google scholar
|
[18] |
Gu W, Lu Y, Tan Z, Xu P, Xie K, Li X, Sun L (2017b). Fungi diversity from different depths and times in chicken manure waste static aerobic composting. Bioresource Technology, 239: 447–453
CrossRef
Google scholar
|
[19] |
Guo Y, Rene E R, Wang J, Ma W (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
CrossRef
Google scholar
|
[20] |
Han Y, Yang T, Chen T, Li L, Liu J (2019). Characteristics of submicron aerosols produced during aeration in wastewater treatment. Science of the Total Environment, 696: 134019
CrossRef
Google scholar
|
[21] |
He P, Du W, Xu X, Zhang H, Shao L, Lu F (2020). Effect of biochemical composition on odor emission potential of biowaste during aerobic biodegradation. Science of the Total Environment, 727: 138285
CrossRef
Google scholar
|
[22] |
He P, Wei S, Shao L, Lu F (2019). Aerosolization behavior of prokaryotes and fungi during composting of vegetable waste. Waste Management (New York, N.Y.), 89: 103–113
CrossRef
Google scholar
|
[23] |
Jiang J, Wang Y, Liu J, Yang X, Ren Y, Miao H, Pan Y, Lv J, Yan G, Ding L, Li Y (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
CrossRef
Google scholar
|
[24] |
Kim I H, Kim K Y, Phae C G, Kim D K(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
CrossRef
Google scholar
|
[25] |
Kohlmeier S, Smits T H M, Ford R M, Keel C, Harms H, Wick L Y (2005). Taking the fungal highway: Mobilization of pollutant-degrading bacteria by fungi. Environmental Science & Technology, 39(12): 4640–4646
CrossRef
Google scholar
|
[26] |
Lainhart W (2018). Fusarium spp., a genus of common plant pathogens that can cause devastating, opportunistic human disease. Clinical Microbiology Newsletter, 40(1): 1–5
CrossRef
Google scholar
|
[27] |
Langarica-Fuentes A, Zafar U, Heyworth A, Brown T, Fox G, Robson G D (2014). Fungal succession in an in-vessel composting system characterized using 454 pyrosequencing. FEMS Microbiology Ecology, 88(2): 296–308
CrossRef
Google scholar
|
[28] |
Li C, Li H, Yao T, Su M, Ran F, Han B, Li J, Lan X, Zhang Y, Yang X, Gun S (2019). Microbial inoculation influences bacterial community succession and physicochemical characteristics during pig manure composting with corn straw. Bioresource Technology, 289: 121653
CrossRef
Google scholar
|
[29] |
Li Y, Liu Y, Yong X, Wu X, Jia H, Wong J W C, Wu H, Zhou J (2020). Odor emission and microbial community succession during biogas residue composting covered with a molecular membrane. Bioresource Technology, 297: 122518
CrossRef
Google scholar
|
[30] |
Lindquist D, Murrill D, Burran W P, Winans G, Janda J M, Probert W (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
CrossRef
Google scholar
|
[31] |
Liu M, Nobu M K, Ren J, Jin X, Hong G, Yao H (2020a). Bacterial compositions in inhalable particulate matters from indoor and outdoor wastewater treatment processes. Journal of Hazardous Materials, 385: 121515
CrossRef
Google scholar
|
[32] |
Liu T, Awasthi S K, Duan Y, Zhang Z, Awasthi M K (2020b). Effect of fine coal gasification slag on improvement of bacterial diversity community during the pig manure composting. Bioresource Technology, 304: 123024
CrossRef
Google scholar
|
[33] |
Lu F, Shao L M, Zhang H, Fu W D, Feng S J, Zhan L T, Chen Y M, He P J (2018). Application of advanced techniques for the assessment of bio-stability of biowaste-derived residues: A minireview. Bioresource Technology, 248: 122–133
CrossRef
Google scholar
|
[34] |
Madamarandawala P, Weerasinghe Y, Pathiraja D, Ekanayake A, Madegedara D, Magana-Arachchi D (2019). Impact of microbial air quality in preschools on paediatric respiratory health. Sn Applied Sciences, 1(10): 1280
CrossRef
Google scholar
|
[35] |
Mbareche H, Veillette M, Bonifait L, Dubuis M E, Benard Y, Marchand G, Bilodeau G J, Duchaine C (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
CrossRef
Google scholar
|
[36] |
Michaud J M, Thompson L R, Kaul D, Espinoza J L, Richter R A, Xu Z Z, Lee C, Pham K M, Beall C M, Malfatti F, Azam F, Knight R, Burkart M D, Dupont C L, Prather K A (2018). Taxon-specific aerosolization of bacteria and viruses in an experimental ocean-atmosphere mesocosm. Nature Communications, 9(1): 2017
CrossRef
Google scholar
|
[37] |
Moletta M, Delgenes J P, Godon J J (2007). Differences in the aerosolization behavior of microorganisms as revealed through their transport by biogas. Science of the Total Environment, 379(1): 75–88
CrossRef
Google scholar
|
[38] |
Moletta-Denat M, Bru-Adan V, Delgenes J P, Hamelin J, Wery N, Godon J J (2010). Selective microbial aerosolization in biogas demonstrated by quantitative PCR. Bioresource Technology, 101(19): 7252–7257
CrossRef
Google scholar
|
[39] |
Niculita-Hirzel H, Hantier G, Storti F, Plateel G, Roger T (2016). Frequent occupational exposure to Fusarium mycotoxins of workers in the swiss grain industry. Toxins, 8(12): 370
CrossRef
Google scholar
|
[40] |
OSHA(Occupational Safety and Health Administration) (1994). “Indoor air quality-proposed rule” notice of proposed rulemaking. Federal Register, 59(65): 15968–16039
|
[41] |
Pahari A K, Dasgupta D, Patil R S, Mukherji S (2016). Emission of bacterial bioaerosols from a composting facility in Maharashtra, India. Waste Management (New York, N.Y.), 53: 22–31
CrossRef
Google scholar
|
[42] |
Pankhurst L J, Whitby C, Pawlett M, Larcombe L D, Mckew B, Deacon L J, Morgan S L, Villa R, Drew G H, Tyrrel S, Pollard S J T, Coulon F (2012). Temporal and spatial changes in the microbial bioaerosol communities in green-waste composting. FEMS Microbiology Ecology, 79(1): 229–239
CrossRef
Google scholar
|
[43] |
Parker B C, Ford M A, Gruft H, Falkinham J O (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] |
Peng J, Wang K, Yin X, Yin X, Du M, Gao Y, Antwi P, Ren N, Wang A (2019). Trophic mode and organics metabolic characteristic of fungal community in swine manure composting. Frontiers of Environmental Science & Engineering, 13(6): 137–146
CrossRef
Google scholar
|
[45] |
Perrott P, Turgeon N, Gauthier-Levesque L, Duchaine C (2017). Preferential aerosolization of bacteria in bioaerosols generated invitro. Journal of Applied Microbiology, 123(3): 688–697
CrossRef
Google scholar
|
[46] |
Ravva S, Sarreal C, Mandrell R (2011). Bacterial communities in aerosols and manure samples from two different dairies in central and sonoma valleys of california. PLoS One, 6(2): e17281
CrossRef
Google scholar
|
[47] |
Robertson S, Douglas P, Jarvis D, Marczylo E (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
CrossRef
Google scholar
|
[48] |
Robledo-Mahón, Gomez-Silvan C, Andersen G L, Calvo C, Aranda E (2020). Assessment of bacterial and fungal communities in a full-scale thermophilic sewage sludge composting pile under a semipermeable cover. Bioresource Technology, 298: 122550
CrossRef
Google scholar
|
[49] |
Robledo-Mahón T, Martin M A, Gutierrez M C, Toledo M, Gonzalez I, Aranda E, Chica A F, Calvo C (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
CrossRef
Google scholar
|
[50] |
Rodriguez-Diaz M, Cerrone F, Sanchez-Peinado M, Santacruz-Calvo L, Pozo C, López J G (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
CrossRef
Google scholar
|
[51] |
Ryan M P, Pembroke J T (2018). Brevundimonas spp: Emerging global opportunistic pathogens. Virulence, 9(1): 480–493
CrossRef
Google scholar
|
[52] |
Shestivska V, Dryahina K, Nunvar J, Sovova K, Elhottova D, Nemec A, Smith D, Spanel P (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
CrossRef
Google scholar
|
[53] |
Springer D J, Saini D, Byrnes E J, Heitman J, Frothingham R (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
CrossRef
Google scholar
|
[54] |
Steger K, Sjögren A M, Jarvis A, Jansson J K, Sundh I (2007). Development of compost maturity and Actinobacteria populations during full-scale composting of organic household waste. Journal of Applied Microbiology, 103(2): 487–498
CrossRef
Google scholar
|
[55] |
Su J Q, Wei B, Ou-Yang W Y, Huang F Y, Zhao Y, Xu H J, Zhu Y G (2015). Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environmental Science & Technology, 49(12): 7356–7363
CrossRef
Google scholar
|
[56] |
Tang Z, Xi B, Huang C, Tan W, Li W, Zhao X, Liu K, Xia X (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
CrossRef
Google scholar
|
[57] |
Veillette M, Bonifait L, Mbareche H, Marchand G, Duchaine C (2018). Preferential aerosolization of Actinobacteria during handling of composting organic matter. Journal of Aerosol Science, 116: 83–91
CrossRef
Google scholar
|
[58] |
Vinzelj J, Joshi A, Insam H, Podmirseg S M (2020). Employing anaerobic fungi in biogas production: Challenges & opportunities. Bioresource Technology, 300: 122687
CrossRef
Google scholar
|
[59] |
Wang J, Liu Z, Xia J, Chen Y (2019). Effect of microbial inoculation on physicochemical properties and bacterial community structure of citrus peel composting. Bioresource Technology, 291: 121843
CrossRef
Google scholar
|
[60] |
Wang Y, Liu L, Yang J, Duan Y, Luo Y, Taherzadeh M J, Li Y, Li H, Awasthi M K, Zhao Z (2020). The diversity of microbial community and function varied in response to different agricultural residues composting. Science of the Total Environment, 715: 136983
CrossRef
Google scholar
|
[61] |
Wei M, Xu C, Xu X, Zhu C, Li J, Lv G (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
CrossRef
Google scholar
|
[62] |
Wei Y, Zhao Y, Wang H, Lu Q, Cao Z, Cui H, Zhu L, Wei Z (2016). An optimized regulating method for composting phosphorus fractions transformation based on biochar addition and phosphate-solubilizing bacteria inoculation. Bioresource Technology, 221: 139–146
CrossRef
Google scholar
|
[63] |
Wick L Y, Remer R, Würz B, Reichenbach J, Braun S, Schäfer F, Harms H (2007). Effect of fungal hyphae on the access of bacteria to phenanthrene in soil. Environmental Science & Technology, 41(2): 500–505
CrossRef
Google scholar
|
[64] |
Yang Y, Yin H, Peng H, Lu G, Dang Z (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
CrossRef
Google scholar
|
[65] |
Zhang H, Sun H, Yang R, Li S, Zhou M, Gao T, An L, Chen X, Dyson P (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
CrossRef
Google scholar
|
[66] |
Zhang L, Jia Y, Zhang X, Feng X, Wu J, Wang L, Chen G (2016b). Wheat straw: an inefficient substrate for rapid natural lignocellulosic composting. Bioresource Technology, 209: 402–406
CrossRef
Google scholar
|
[67] |
Zhao X, Wei Y, Zhang F, Tan W, Fan Y, Xi B (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
CrossRef
Google scholar
|
[68] |
Zhou G, Xu X, Qiu X, Zhang J (2019). Biochar influences the succession of microbial communities and the metabolic functions during rice straw composting with pig manure. Bioresource Technology, 272: 10–18
CrossRef
Google scholar
|
[69] |
Zhou H B, Ma C, Gao D, Chen T B, Zheng G D, Chen J, Pan T H (2014). Application of a recyclable plastic bulking agent for sewage sludge composting. Bioresource Technology, 152: 329–336
CrossRef
Google scholar
|
[70] |
Zittel R, Da Silva C P, Domingues C E, Seremeta D C H, Da Cunha K M, De Campos S X (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
CrossRef
Google scholar
|
/
〈 | 〉 |