Abstract
Fungi are important contributors to the various functions of activated sludge wastewater treatment plants (WWTPs); however, the diversity and geographic characteristics of fungal populations have remained vastly unexplored. Here, quantitative polymerase chain reaction and 454 pyrosequencing were combined to investigate the abundance and diversity of the activated sludge fungal communities from 18 full-scale municipal WWTPs in China. Phylogenetic taxonomy revealed that the members of the fungal communities were assigned to 7 phyla and 195 genera. Ascomycota and Basidiomycota were the most abundant phyla, dominated by Pluteus, Wickerhamiella, and Penicillium. Twenty-three fungal genera, accounting for 50.1 % of the total reads, were shared by 18 WWTPs and constituted a core fungal community. The fungal communities presented similar community diversity but different community structures across the WWTPs. Significant distance decay relationships were observed for the dissimilarity in fungal community structure and altitudinal distance between WWTPs. Additionally, the community evenness increased from 0.25 to 0.7 as the altitude increased. Dissolved oxygen and the C/N ratio were determined to be the most dominant contributors to the variation in fungal community structure via redundancy analysis. The observed data demonstrated the diverse occurrence of fungal species and gave a marked view of fungal community characteristics based on the previously unexplored fungal communities in activated sludge WWTPs.
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Alby-Laurent F, Dollfus C, Ait-Oufella H, Rambaud J, Legrand O et al (2016) Trichosporon: another yeast-like organism responsible for immune reconstitution inflammatory syndrome in patients with hematological malignancy. Hematol Oncol doi. doi:10.1002/hon.2309
Awad FM, Kraume M (2011a) Keratinophilic fungi in activated sludge of wastewater treatment plants with MBR in Berlin, Germany. Int J Environ Health Res 4:244–253
Awad MF, Kraume M (2011b) Fungal diversity in activated sludge from membrane bioreactors in Berlin. Can J Microbiol 57:693–698
Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555
Basu S, Tilak R, Kumar A (2015) Multidrug-resistant Trichosporon: an unusual fungal sepsis in preterm neonates. Pathog Glob Health 109:202–206
Cho O, Matsukura M, Sugita T (2015) Molecular evidence that the opportunistic fungal pathogen Trichosporon asahii is part of the normal fungal microbiota of the human gut based on rRNA genotyping. Int J Infect Dis 39:87–88
Cooke WB, Pipes WO (1970) The occurrence of fungi in activated sludge. Mycopathol Mycol Appl 40:249–250
Davey ML, Heegaard E, Halvorsen R, Ohlson M, Kauserud H (2012) Seasonal trends in the biomass and structure of bryophyte-associated fungal communities explored by 454 pyrosequencing. New Phytol 195:844–856
De Gannes V, Eudoxie G, Hickey WJ (2013) Insights into fungal communities in composts revealed by 454-pyrosequencing: implications for human health and safety. Front Microbiol 4:164
Espindola A, Schneider W, Hoyt PR, Marek SM, Garzon C (2015) A new approach for detecting fungal and oomycete plant pathogens in next generation sequencing metagenome data utilising electronic probes. Int J Data Min Bioinform 12:115–128
Evans TN, Seviour RJ (2012) Estimating biodiversity of fungi in activated sludge communities using culture-independent methods. Microb Ecol 63:773–786
Felczak A, Bernat P, Rozalska S, Lisowska K (2016) Quinoline biodegradation by filamentous fungus Cunninghamella elegans and adaptive modifications of the fungal membrane composition. Environ Sci Pollut Res Int 23:8872–8880
Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM et al (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Fredriksson NJ, Hermansson M, Wilen BM (2012) Diversity and dynamics of Archaea in an activated sludge wastewater treatment plant. BMC Microbiol 12:140
Freeman KR, Martin AP, Karki D, Lynch RC, Mitter MS et al (2009) Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci U S A 106:18315–18320
Glynou K, Ali T, Buch AK, Kia SH, Ploch S et al (2015) The local environment determines the assembly of root endophytic fungi at a continental scale. Environ Microbiol 18:2418–2434
Guest RK, Smith DW (2002) A potential new role for fungi in a wastewater MBR biological nitrogen reduction system. J Environ Eng Sci 1:433–437
Hashimoto K, Matsuda M, Inoue D, Ike M (2014) Bacterial community dynamics in a full-scale municipal wastewater treatment plant employing conventional activated sludge process. J Biosci Bioeng 118:64–71
Hayden CJ, Beman JM (2016) Microbial diversity and community structure along a lake elevation gradient in Yosemite National Park, California, USA. Environ Microbiol 18:1782–1791
Hossain F (2004) Activated sludge bulking: a review of causes and control strategies. J Instit Eng (INDIA) 85:1–6
Huang SH, Wu CH, Chang YC, Kwon-Chung KJ, Brown RJ et al (2012) Cryptococcus neoformans-derived microvesicles enhance the pathogenesis of fungal brain infection. PLoS One 7:e48570
Kacprzak M, Neczaj E, Okoniewska E (2005) The comparative mycological analysis of wastewater and sewage sludges from selected wastewater treatment plants. Desalination 185:363–370
Lakshmi V, Das N (2013) Removal of caffeine from industrial wastewater using Trichosporon asahii. J Environ Biol 34:701–708
Langarica-Fuentes A, Zafar U, Heyworth A, Brown T, Fox G et al (2014) Fungal succession in an in-vessel composting system characterized using 454 pyrosequencing. FEMS Microbiol Ecol 88:296–308
Lee SH, Kang HJ, Park HD (2015) Influence of influent wastewater communities on temporal variation of activated sludge communities. Water Res 73:132–144
Liu S, Hou Y, Sun G (2013) Synergistic degradation of pyrene and volatilization of arsenic by cocultures of bacteria and a fungus. Front Environ Sci Eng 7:191–199
Liu M, Zhang X, Tan T (2016) The effect of amino acids on lipid production and nutrient removal by Rhodotorula glutinis cultivation in starch wastewater. Bioresour Technol 218:712–717
Mannan S, Fakhru'l-Razi A, Alam MZ (2005) Use of fungi to improve bioconversion of activated sludge. Water Res 39:2935–2943
Manolakaki D, Velmahos G, Kourkoumpetis T, Chang Y, Alam HB et al (2010) Candida infection and colonization among trauma patients. Virulence 1:367–375
Meng H, Li K, Nie M, Wan JR, Quan ZX et al (2013) Responses of bacterial and fungal communities to an elevation gradient in a subtropical montane forest of China. Appl Microbiol Biotechnol 97:2219–2230
Menolli N Jr, Capelari M (2010) Notes on Pluteus (Pluteaceae, Agaricales) from Brazil including two new species and a new record. Mycologia 102:697–707
Merlin C, Devers M, Crouzet O, Heraud C, Steinberg C et al (2014) Characterization of chlordecone-tolerant fungal populations isolated from long-term polluted tropical volcanic soil in the French West Indies. Environ Sci Pollut Res Int 21:4914–4927
Nhi-Cong le T, Mai CT, Minh NN, Ha HP, Lien do T et al (2016) Degradation of sec-hexylbenzene and its metabolites by a biofilm-forming yeast Trichosporon asahii B1 isolated from oil-contaminated sediments in Quangninh coastal zone, Vietnam. J Environ Sci Heal A 51:267–275
Niazi S, Hassanvand MS, Mahvi AH, Nabizadeh R, Alimohammadi M et al (2015) Assessment of bioaerosol contamination (bacteria and fungi) in the largest urban wastewater treatment plant in the Middle East. Environ Sci Pollut Res Int 22:16014–16021
Niu L, Li Y, Wang P, Zhang W, Wang C et al (2015) Understanding the linkage between elevation and the activated-sludge bacterial community along a 3,600-meter elevation gradient in China. Appl Environ Microb 81:6567–6576
Ofiteru ID, Lunn M, Curtis TP, Wells GF, Criddle CS et al (2010) Combined niche and neutral effects in a microbial wastewater treatment community. Proc Natl Acad Sci U S A 107:15345–15350
Peay KG, Bruns TD (2014) Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant-fungal interactions. New Phytol 204:180–191
Peng RH, Xiong AS, Xue Y, Fu XY, Gao F et al (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955
Pikart TG, Souza GK, Costa VA, Hansson C, Zanuncio JC (2011) Paracrias pluteus (Hymenoptera, Eulophidae) in Brazil: new distribution and host records, and with a new host group for Paracrias. Zookeys 102:77–82
Purnomo AS, Putra SR, Shimizu K, Kondo R (2014) Biodegradation of heptachlor and heptachlor epoxide-contaminated soils by white-rot fungal inocula. Environ Sci Pollut Res Int 21:11305–11312
Santos C, Lucas MS, Dias AA, Bezerra RM, Peres JA et al (2014) Winery wastewater treatment by combination of Cryptococcus laurentii and Fenton's reagent. Chemosphere 117:53–58
Singh D, Takahashi K, Kim M, Chun J, Adams JM (2012) A hump-backed trend in bacterial diversity with elevation on Mount Fuji, Japan. Microb Ecol 63:429–437
Soomro IH, Zardari M, Yasmeen FK, Abro H (2007) Keratinolytic mycoflaora from the sludge in Khairpur, Sindh, Pakistan. Pak J Bot 39:2625–2627
Sugimori D (2009) Edible oil degradation by using yeast coculture of Rhodotorula pacifica ST3411 and Cryptococcus laurentii ST3412. Appl Microbiol Biotechnol 82:351–357
Verstrepen KJ, Klis FM (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60:5–15
Wang X, Hu M, Xia Y, Wen X, Ding K (2012) Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl Environ Microb 78:7042–7047
Weaver B, Wuensch KL (2013) SPSS and SAS programs for comparing Pearson correlations and OLS regression coefficients. Behav Res Methods 45:880–895
Weber SD, Hofmann A, Pilhofer M, Wanner G, Agerer R et al (2009a) The diversity of fungi in aerobic sewage granules assessed by 18S rRNA gene and ITS sequence analyses. FEMS Microbiol Ecol 68:246–254
Wells GF, Park HD, Eggleston B, Francis CA, Criddle CS (2011) Fine-scale bacterial community dynamics and the taxa-time relationship within a full-scale activated sludge bioreactor. Water Res 45:5476–5488
Yang Y, Gao Y, Wang S, Xu D, Yu H et al (2014) The microbial gene diversity along an elevation gradient of the Tibetan grassland. The ISME J 8:430–440
Zabalaga J, Amy G, von Munch E (2007) Evaluation of agricultural reuse practices and relevant guidelines for the Alba Rancho WWTP (primary and secondary facultative ponds) in Cochabamba, Bolivia. Water Sci Technol 55:469–475
Zhang J, Zeng G, Chen Y, Yu M, Yu Z et al (2011) Effects of physico-chemical parameters on the bacterial and fungal communities during agricultural waste composting. Bioresour Technol 102:2950–2956
Zhang H, Huang T, Chen S (2015) Ignored sediment fungal populations in water supply reservoirs are revealed by quantitative PCR and 454 pyrosequencing. BMC Microbiol 15:44
Acknowledgements
This study was supported by the National Natural Science Foundation of China (nos. 51322901, 91547105, and 51568059), the Foundation for Innovative Research Groups of the National Natural Science Foundation of China (51421006), the Fundamental Research Funds for the Central Universities (2016B10614), PAPD, and TAPP.
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Niu, L., Li, Y., Xu, L. et al. Ignored fungal community in activated sludge wastewater treatment plants: diversity and altitudinal characteristics. Environ Sci Pollut Res 24, 4185–4193 (2017). https://doi.org/10.1007/s11356-016-8137-4
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DOI: https://doi.org/10.1007/s11356-016-8137-4