Bioaerosolization behavior along sewage sludge biostabilization

Abstract

• 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.

Graphical abstract

Keywords

Sludge / Composting / Bioaerosol / Bioaerosolization index / High-throughput sequencing / 4′, 6-diamidino-2-phenylindole (DAPI)

References

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[51] Ryan M P, Pembroke J T (2018). Brevundimonas spp: Emerging global opportunistic pathogens. Virulence, 9(1): 480–493

[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

[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

[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

[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

[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

[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

[58] Vinzelj J, Joshi A, Insam H, Podmirseg S M (2020). Employing anaerobic fungi in biogas production: Challenges & opportunities. Bioresource Technology, 300: 122687

[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

[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

[61] Wei M, Xu C, Xu X, Zhu C, Li J, Lv G (2019). Characteristics of atmospheric bacterial and fungal communities in PM_2.5 following biomass burning disturbance in a rural area of North China Plain. Science of the Total Environment, 651: 2727–2739

[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

[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

[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

[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

[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

[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

[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

[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

[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

RIGHTS & PERMISSIONS

Higher Education Press