Fungal diversity and its mechanism of community shaping in the milieu of sanitary landfill

doi:10.1007/s11783-020-1370-6

Front. Environ. Sci. Eng.

2021, Vol. 15

Issue (4) : 77 https://doi.org/10.1007/s11783-020-1370-6

RESEARCH ARTICLE

Fungal diversity and its mechanism of community shaping in the milieu of sanitary landfill

Rong Ye¹, Sai Xu², Qian Wang¹, Xindi Fu¹, Huixiang Dai¹, Wenjing Lu¹(

)

¹. School of Environment, Tsinghua University, Beijing 100084, China
². Jiangsu Key Laboratory of Chemical Pollution Control and Resources Reuse, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210094, China

Download: PDF(1338 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

• Ascomycota was the predominant phylum in sanitary landfill fungal communities.

• Saprophytic fungi may be of special importance in landfill ecology.

• Both richness and diversity of fungal community were lower in leachate than refuse.

• Physical habitat partly contributed to the geographic variance of fungal community.

• NO₃⁻ was considered the most significant abiotic factor shaping fungal community.

Land filling is the main method to dispose municipal solid waste in China. During the decomposition of organic waste in landfills, fungi play an important role in organic carbon degradation and nitrogen cycling. However, fungal composition and potential functions in landfill have not yet been characterized. In this study, refuse and leachate samples with different areas and depths were taken from a large sanitary landfill in Beijing to identify fungal communities in landfills. In high-throughput sequencing of ITS region, 474 operational taxonomic units (OTUs) were obtained from landfill samples with a cutoff level of 3% and a sequencing depth of 19962. The results indicates that Ascomycota, with the average relative abundance of 84.9%, was the predominant phylum in landfill fungal communities. At the genus level, Family Hypocreaceae unclassified (15.7%), Fusarium (9.9%) and Aspergillus (8.3%) were the most abundant fungi found in the landfill and most of them are of saprotrophic lifestyle, which plays a big role in nutrient cycling in ecosystem. Fungi existed both in landfilled refuse and leachate while both the richness and evenness of fungal communities were higher in the former. In addition, fungal communities in landfilled refuse presented geographic variances, which could be partly attributed to physical habitat properties (pH, dissolved organic carbon, volatile solid, NH₄⁺, NO₂⁻ and NO₃⁻), while NO₃⁻ was considered the most significant factor (p<0.05) in shaping fungal community.

Keywords Sanitary landfill Fungal community Diversity Saprotroph Physical habitat Environmental factor

Corresponding Author(s): Wenjing Lu

Issue Date: 25 November 2020

Cite this article:

Rong Ye,Sai Xu,Qian Wang, et al. Fungal diversity and its mechanism of community shaping in the milieu of sanitary landfill[J]. Front. Environ. Sci. Eng., 2021, 15(4): 77.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-020-1370-6
https://academic.hep.com.cn/fese/EN/Y2021/V15/I4/77

Tab.1 Sampling scheme

Fig.1 pH variation (a) and dissolved organic carbon (DOC) concentrations (b) of refuse samples (A, B, C) and leachate samples (AL, CL) from different depth of a landfill. Small letters above bars indicate significant difference among parameter values of different refuse samples and capital letters indicate significant difference among different leachate samples.

Fig.2 The concentrations of ammonia (a), nitrite (b) and nitrate (c) in refuse samples (A, B, C) and leachate samples (AL, CL) from different depth of the landfill. Small letters above bars indicate significant difference among parameter values of different refuse samples and capital letters indicate significant difference among different leachate samples.

Fig.3 Species accumulation curve (a) and the alpha diversity-Chao index (b) and Shannon index (c) -of fungal communities in landfill.

Fig.4 Relative abundance of top 20 genera (average relative abundance>1%) of fungal communities in refuse samples (a) and leachate samples (b).

Fig.5 The relative abundance of different tropic modes (Pathotroph, Saproroph and Symbiotroph) of fungi among landfill communities; the data was obtained from the probable and high probable classification via FUNGuild. Sa/Pa denotes the ratio of saprotroph to pathotroph.

Fig.6 (a) Nonmetric multidimensional scaling (NMDS) analysis of fungal communities in landfill samples based on “Bray–Curtis” distance. Dashed circle means confidence level of 0.68, representing 68% of fungal community. (b) Redundancy analysis (RDA) of relationships between fungal communities and environmental factors (pH, VS, DOC, ammonia, nitrite, and nitrate) in landfill refuse samples.

1	P Baldrian, M Kolarik, M Stursova, J Kopecky, V Valaskova, T Vetrovsky, L Zifcakova, J Snajdr, J Ridl, C Vlcek, J Voriskova (2012). Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME Journal, 6(2): 248–258 https://doi.org/10.1038/ismej.2011.95
2	S C Bolyard, D R Reinhart (2016). Application of landfill treatment approaches for stabilization of municipal solid waste. Waste Management (New York, N.Y.), 55: 22–30 https://doi.org/10.1016/j.wasman.2016.01.024
3	G Braker, R Conrad (2011). Diversity, structure, and size of N2O-producing microbial communities in soils: What matters for their functioning? Advances in Applied Microbiology, 75: 33–70 https://doi.org/10.1016/B978-0-12-387046-9.00002-5
4	A Chao (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11(4): 265–270
5	H Chen, F Yu, W Shi (2016). Detection of N2O-producing fungi in environment using nitrite reductase gene (nirK)-targeting primers. Fungal Biology, 120(12): 1479–1492 https://doi.org/10.1016/j.funbio.2016.07.012
6	K Dou, J Gao, C Zhang, H Yang, X Jiang, J Li, Y Li, W Wang, H Xian, S Li, Y Liu, J Hu, J Chen (2019). Trichoderma biodiversity in major ecological systems of China. Journal of Microbiology (Seoul, Korea), 57(8): 668–675 https://doi.org/10.1007/s12275-019-8357-7
7	EPM (Ministry of Environmental and Protection of the People’s Republic of China) (2012). Soil-Determination of ammonium, nitrite and nitrate by extraction with potassium chloride solution-spectrophotometric methods. HJ 634–2012. Beijing: China Environmental Science Press (in Chinese)
8	C Farkas, J M Rezessy-Szabo, V K Gupta, D H Truong, L Friedrich, J Felfoldi, Q D Nguyen (2019). Microbial saccharification of wheat bran for bioethanol fermentation. Journal of Cleaner Production, 240: 118269 https://doi.org/10.1016/j.jclepro.2019.118269
9	N Fierer, Z Liu, M Rodriguez-Hernandez, R Knight, M Henn, M T Hernandez (2008). Short-term temporal variability in airborne bacterial and fungal populations. Applied and Environmental Microbiology, 74(1): 200–207 https://doi.org/10.1128/AEM.01467-07
10	M Hayatsu, K Tago, M Saito (2008). Various players in the nitrogen cycle: Diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Science and Plant Nutrition, 54(1): 33–45 https://doi.org/10.1111/j.1747-0765.2007.00195.x
11	Y Li, S J Chapman, G W Nicol, H Yao (2018). Nitrification and nitrifiers in acidic soils. Soil Biology & Biochemistry, 116: 290–301 https://doi.org/10.1016/j.soilbio.2017.10.023
12	R Liu, H Suter, J He, H Hayden, D Chen (2015). Influence of temperature and moisture on the relative contributions of heterotrophic and autotrophic nitrification to gross nitrification in an acid cropping soil. Journal of Soils and Sediments, 15(11): 2304–2309 https://doi.org/10.1007/s11368-015-1170-y
13	S Liu, H Wang, P Tian, X Yao, H Sun, Q Wang, M Delgado-Baquerizo (2020). Decoupled diversity patterns in bacteria and fungi across continental forest ecosystems. Soil Biology & Biochemistry, 144: 107763 https://doi.org/10.1016/j.soilbio.2020.107763
14	R J Lockhart, M I Van Dyke, I R Beadle, P Humphreys, A J McCarthy (2006). Molecular biological detection of anaerobic gut fungi (Neocallimastigales) from landfill sites. Applied and Environmental Microbiology, 72(8): 5659–5661 https://doi.org/10.1128/AEM.01057-06
15	K Maeda, S Toyoda, L Philippot, S Hattori, K Nakajima, Y Ito, N Yoshida (2017). Relative contribution of nirK- and nirS- bacterial denitrifiers as well as fungal denitrifiers to nitrous oxide production from dairy manure compost. Environmental Science & Technology, 51(24): 14083–14091 https://doi.org/10.1021/acs.est.7b04017
16	J Moore-Kucera, S B Cox, M Peyron, G Bailes, K Kinloch, K Karich, C Miles, D A Inglis, M Brodhagen (2014). Native soil fungi associated with compostable plastics in three contrasting agricultural settings. Applied Microbiology and Biotechnology, 98(14): 6467–6485 https://doi.org/10.1007/s00253-014-5711-x
17	N Mothapo, H Chen, M A Cubeta, J M Grossman, F Fuller, W Shi (2015). Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy. Soil Biology & Biochemistry, 83: 160–175 https://doi.org/10.1016/j.soilbio.2015.02.001
18	E Munir, R S M Harefa, N Priyani, D Suryanto (2018). Plastic degrading fungi Trichoderma viride and Aspergillus nomius isolated from local landfill soil in Medan. IOP Conference Series: Earth and Environmental Science, 126: 012145 https://doi.org/10.1088/1755-1315/126/1/012145
19	NBSC (National Bureau of Statistics of China) (2019). China Statistical Yearbook 2019. Beijing: China Statistics Press (in Chinese)
20	J Peng, K Wang, X B Yin, X Q Yin, M F Du, Y Z Gao, P Antwi, N Q Ren, A J Wang (2019). Trophic mode and organics metabolic characteristic of fungal community in swine manure composting. Frontiers of Environmental Science & Engineering, 13(6): 93 https://doi.org/10.1007/s11783-019-1177-5
21	T A Richards, M D M Jones, G Leonard, D Bass (2012). Marine fungi: Their ecology and molecular diversity. Annual Review of Marine Science, 4: 495–522 https://doi.org/10.1146/annurev-marine-120710-100802
22	N N Sang, S Soda, T Ishigaki, M Ike (2012). Microorganisms in landfill bioreactors for accelerated stabilization of solid wastes. Journal of Bioscience and Bioengineering, 114(3): 243–250 https://doi.org/10.1016/j.jbiosc.2012.04.007
23	C W Schadt, A P Martin, D A Lipson, S K Schmidt (2003). Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science, 301(5638): 1359–1361 https://doi.org/10.1126/science.1086940
24	L Sekhohola-Dlamini, M Tekere (2020). Microbiology of municipal solid waste landfills: A review of microbial dynamics and ecological influences in waste bioprocessing. Biodegradation, 31: 1–21 https://doi.org/10.1007/s10532-019-09890-x
25	C E Shannon (1948). A mathematical theory of communication. Bell System Technical Journal, 27(3): 379–423 https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
26	F Spina, C Cordero, T Schiliro, B Sgorbini, C Pignata, G Gilli, C Bicchi, G C Varese (2015). Removal of micropollutants by fungal laccases in model solution and municipal wastewater: evaluation of estrogenic activity and ecotoxicity. Journal of Cleaner Production, 100: 185–194 https://doi.org/10.1016/j.jclepro.2015.03.047
27	J M Talbot, T D Bruns, D P Smith, S Branco, S I Glassman, S Erlandson, R Vilgalys, K G Peay (2013). Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biology & Biochemistry, 57: 282–291 https://doi.org/10.1016/j.soilbio.2012.10.004
28	R Varnaitė , V Raudonienė, D Bridžiuvienė (2011). Enzymatic biodegradation of lignin-cellulose complex in plant origin material. Materials Science-Medziagotyra, 17(1): 99–103 https://doi.org/10.5755/j01.ms.17.1.258
29	K Wang, H Mao, X Li (2018). Functional characteristics and influence factors of microbial community in sewage sludge composting with inorganic bulking agent. Bioresource Technology, 249: 527–535 https://doi.org/10.1016/j.biortech.2017.10.034
30	S Xu, W Lu, Y Liu, Z Ming, Y Liu, R Meng, H Wang (2017). Structure and diversity of bacterial communities in two large sanitary landfills in China as revealed by high-throughput sequencing (MiSeq). Waste Management (New York, N.Y.), 63: 41–48 https://doi.org/10.1016/j.wasman.2016.07.047
31	N Yilmaz, C A López-Quintero, A M Vasco-Palacios, J C Frisvad, B Theelen, T Boekhout, R A Samson, J Houbraken (2016). Four novel Talaromyces species isolated from leaf litter from Colombian Amazon rain forests. Mycological Progress, 15(10–11): 1041–1056 https://doi.org/10.1007/s11557-016-1227-3
32	K Yokoyama, K Jinnai, Y Sakiyama, M Touma (2012). Contribution of fungi to acetylene-tolerant and high ammonia availability-dependent nitrification potential in tea field soils with relatively neutral pH. Applied Soil Ecology, 62: 37–41 https://doi.org/10.1016/j.apsoil.2012.07.008
33	U Zafar, A Houlden, G D Robson (2013). Fungal communities associated with the biodegradation of polyester polyurethane buried under compost at different temperatures. Applied and Environmental Microbiology, 79(23): 7313–7324 https://doi.org/10.1128/AEM.02536-13
34	X Zhang, Y Zhong, S Yang, W Zhang, M Xu, A Ma, G Zhuang, G Chen, W Liu (2014). Diversity and dynamics of the microbial community on decomposing wheat straw during mushroom compost production. Bioresource Technology, 170: 183–195 https://doi.org/10.1016/j.biortech.2014.07.093
35	T Zhu, T Meng, J Zhang, W Zhong, C Müller, Z Cai (2015). Fungi-dominant heterotrophic nitrification in a subtropical forest soil of China. Journal of Soils and Sediments, 15(3): 705–709 https://doi.org/10.1007/s11368-014-1048-4

[1]

FSE-20143-OF-YR_suppl_1

Download

[1]	Guanyu Jiang, Can Wang, Lu Song, Xing Wang, Yangyang Zhou, Chunnan Fei, He Liu. Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster[J]. Front. Environ. Sci. Eng., 2021, 15(3): 46-.
[2]	Min Gao, Ziye Yang, Yajie Guo, Mo Chen, Tianlei Qiu, Xingbin Sun, Xuming Wang. The size distribution of airborne bacteria and human pathogenic bacteria in a commercial composting plant[J]. Front. Environ. Sci. Eng., 2021, 15(3): 39-.
[3]	Chunhong Chen, Hong Liang, Dawen Gao. Community diversity and distribution of ammonia-oxidizing archaea in marsh wetlands in the black soil zone in North-east China[J]. Front. Environ. Sci. Eng., 2019, 13(4): 58-.
[4]	Yanqing Duan, Aijuan Zhou, Kaili Wen, Zhihong Liu, Wenzong Liu, Aijie Wang, Xiuping Yue. Upgrading VFAs bioproduction from waste activated sludge via co-fermentation with soy sauce residue[J]. Front. Environ. Sci. Eng., 2019, 13(1): 3-.
[5]	Yu Miao, Nicholas W. Johnson, Kimberly Heck, Sujin Guo, Camilah D. Powell, Thien Phan, Phillip B. Gedalanga, David T. Adamson, Charles J. Newell, Michael S. Wong, Shaily Mahendra. Microbial responses to combined oxidation and catalysis treatment of 1,4-dioxane and co-contaminants in groundwater and soil[J]. Front. Environ. Sci. Eng., 2018, 12(5): 2-.
[6]	Yujiao Sun, Juanjuan Zhao, Lili Chen, Yueqiao Liu, Jiane Zuo. Methanogenic community structure in simultaneous methanogenesis and denitrification granular sludge[J]. Front. Environ. Sci. Eng., 2018, 12(4): 10-.
[7]	Tingting Fang, Ruisong Pan, Jing Jiang, Fen He, Hui Wang. Effect of salinity on community structure and naphthalene dioxygenase gene diversity of a halophilic bacterial consortium[J]. Front. Environ. Sci. Eng., 2016, 10(6): 16-.
[8]	Xuewei QI,Ke LI,Walter D. POTTER. Estimation of distribution algorithm enhanced particle swarm optimization for water distribution network optimization[J]. Front. Environ. Sci. Eng., 2016, 10(2): 341-351.
[9]	Michael Bruce BECK, Rodrigo VILLARROEL WALKER. On water security, sustainability, and the water-food-energy-climate nexus[J]. Front Envir Sci Eng, 2013, 7(5): 626-639.
[10]	Wuren HUANG, Zhihui BAI, Daniel HOEFEL, Qing HU, Xin LV, Guoqiang ZHUANG, Shengjun XU, Hongyan QI, Hongxun ZHANG. Effects of cotton straw amendment on soil fertility and microbial communities[J]. Front Envir Sci Eng, 2012, 6(3): 336-349.
[11]	Yang GAO, Chiyuan MIAO, Jun XIA, Liang MAO, Yafeng WANG, Pei ZHOU. Plant diversity reduces the effect of multiple heavy metal pollution on soil enzyme activities and microbial community structure[J]. Front Envir Sci Eng, 2012, 6(2): 213-223.
[12]	Bo WEI. Diversity and distribution of proteorhodopsin-containing microorganisms in marine environments[J]. Front Envir Sci Eng, 2012, 6(1): 98-106.
[13]	Zhili HE, Joy D. VAN NOSTRAND, Ye DENG, Jizhong ZHOU. Development and applications of functional gene microarrays in the analysis of the functional diversity, composition, and structure of microbial communities[J]. Front Envir Sci Eng Chin, 2011, 5(1): 1-20.
[14]	Hongyuan WANG, Xiaolu JIANG, Ya HE, Huashi GUAN. Spatial and seasonal variations in bacterial communities of the Yellow Sea by T-RFLP analysis[J]. Front Envir Sci Eng Chin, 2009, 3(2): 194-199.
[15]	ZHAO Yangguo, WANG Aijie, REN Nanqi, ZHAO Yan. Microbial community structure in different wastewater treatment processes characterized by single-strand conformation polymorphism (SSCP) technique[J]. Front.Environ.Sci.Eng., 2008, 2(1): 116-121.

Viewed

Full text

Abstract

Cited

Shared

Discussed