Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (5): 1121-1136    DOI: 10.1016/S2095-3119(20)63341-X
Special Focus: Resource utilization of agricultural solid waste Advanced Online Publication | Current Issue | Archive | Adv Search |
Dynamics of microbial diversity during the composting of agricultural straw
CHANG Hui-qing1, ZHU Xiao-hui1, WU Jie1, GUO Da-yong1, ZHANG Lian-he1, FENG Yao
1 Henan University of Science and Technology, Luoyang 471023, P.R.China
2 Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences/Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture and Rural Affairs, Beijing 100081, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

本研究采用高通量测序法,对添加添加剂的农作物秸秆好氧堆肥过程(升温、高温、降温和腐熟四个阶段)中微生物多样性动态变化进行研究。此外,还对堆肥过程中理化参数的变化进行分析。添加尿素或尿素与微生物菌剂配合添加,可延长堆体高温发酵时间。C/N比和发芽指数变化表明,添加剂直接改变了堆肥的理化性质,影响了细菌和真菌的多样性和丰富度,有利于堆肥化。在高温阶段,秸秆中添加尿素+微生物制剂处理(SNW),其真菌和细菌丰度(OTU)、多样性指数(Shannon)和丰富度指数(Chao)较单独秸秆处理(S)显著增加。不同堆肥阶段,细菌和真菌门、属两级优势菌的相对丰度存在差异。在高温阶段,厚壁菌门和变形菌门的丰度依次为SNW>SN>S。葡萄球菌属、芽孢杆菌属和热裂菌属在中温阶段的丰度顺序相同。子囊菌占真菌总序列的92%以上。随着堆肥过程的进程,子囊菌的丰度逐渐降低。子囊菌在高温期的丰度顺序为S>SN>SNW。曲霉属的丰度占真菌总丰度的4-59%,并在前两个采样周期内丰度增加。曲霉丰度大小顺序为SNW>SN>S。此外,主成分分析(PCA)表明,稻草和稻草+尿素处理的群落组成相似,中温期(第1天)S、SN和SNW处理的细菌群落与其他3个阶段(分别在第5、11和19天)观察到的细菌群落不同,而真菌群落在堆肥过程只表现出轻微的变化。典型相关分析(CCA)和冗余分析(RDA)表明,总碳(TC)、NO3-N(NN)、电导率(EC)和pH值与群落组成高度相关。因此,本研究表明添加剂有助于农作物秸秆堆肥腐熟,并且有利于堆肥品质的改善




Abstract  
The dynamic changes in microbial diversity during the aerobic composting of agricultural crop straw with additives were evaluated using high-throughput sequencing at four phases of composting (mesophilic, thermophilic, cooling and maturation phases).  In addition, the physicochemical parameters of the composting system were determined in this study.  The fermentation time of the thermophilic period was prolonged with the addition of urea or urea combined with a microbial agent.  The ratio of C/N and germination index variation indicated that the additives were favorable for composting, because the additives directly changed the physicochemical properties of the compost and had effects on the diversity and abundance of bacteria and fungi.  The abundance of operational taxonomic units (OTUs), diversity index (Shannon) and richness index (Chao1) of fungi and bacteria were found to significantly increase when urea+microbial agents  were added to straw in the thermophilic phase.  The relative abundance of the predominant bacteria and fungi at the phylum and genus levels differed during different composting phases.  The abundance of the phyla Firmicutes and Proteobacteria declined in the order of treatments SNW>SN>S (S is straw only compost; SN is straw+5 kg t–1 urea compost; and SNW is straw+5 kg t–1 urea+1 kg t–1 microbial agent compost) in the thermophilic phase.  The abundance of the genera Staphylococcus, Bacillus and Thermobifida followed the same order in the mesophilic phase.  Ascomycota accounted for more than 92% of the total fungal sequences.  With the progression of the composting process, the abundance of Ascomycota decreased gradually.  The abundance of Ascomycota followed the order of S>SN>SNW during the thermophilic phase.  The abundance of Aspergillus accounted for 4–59% of the total abundance of fungi and increased during the first two sampling periods.  Aspergillus abundance followed the order of SNW>SN>S.  Additionally, principal component analysis (PCA) revealed that the community compositions in the straw and straw+urea treatments were similar, and that the bacterial communities in treatments S, SN and SNW in the mesophilic phase (at day 1) were different from those observed in three other phases (at days 5, 11, and 19, respectively), while the fungal communities showed only slight variations in their structure in response to changes in the composting process.  Canonical correlation analysis (CCA) and redundancy analysis (RDA) showed that total carbon (TC), NO3-N (NN), electrical conductivity (EC) and pH were highly correlated with community composition.  Therefore, this study highlights that the additives are beneficial to straw composting and result in good quality compost.
 
Keywords:  crop straws        microbial diversity        community composition        dynamic characteristics        high-throughput sequencing  
Received: 24 April 2020   Accepted:
Fund: The authors are thankful for foundation support from the National Key R&D Program of China (2017YFD0801304) and the National Natural Science Foundation of China (31972943).
Corresponding Authors:  Correspondence FENG Yao, Tel: +86-10-82108657, E-mail: fengyao73@126.com   
About author:  CHANG Hui-qing, Tel: +86-379-62836240, E-mail: hqchang@126.com;

Cite this article: 

CHANG Hui-qing, ZHU Xiao-hui, WU Jie, GUO Da-yong, ZHANG Lian-he, FENG Yao. 2021. Dynamics of microbial diversity during the composting of agricultural straw. Journal of Integrative Agriculture, 20(5): 1121-1136.

Abdel-Wareth M T A. 2017. Fungal applications in sustainable environmental biotechnology. International Journal of Environmental Studies, 74, 1049–1050.
Adrian L, Urooj Z, Alan H. 2014. Fungal succession in an in-vessel composting system characterized using 454 pyrosequencing. FEMS Microbiology Ecology, 88, 296–308.
Alok K P, Sunita G, Arif A, Lata N. 2009. Effect of bioaugmentation and nitrogen supplementation on composting of paddy straw. Biodegradation, 20, 293–306.
Antunes L P, Martins L F, Pereira R V. 2016. Microbial community structure and dynamics in thermophilic composting viewed through metagenomics and metatranscriptomics. Scientific Reports, 6, 38915.
Awasthi M K, Li J, Kumar S, Awasthi S K, Wang Q, Chen H, Wang M, Ren X, Zhang Z. 2017. Effects of biochar amendment on bacterial and fungal diversity for co-composting of gelatin industry sludge mixed with organic fraction of municipal solid waste. Bioresource Technology, 246, 214–223.
Bao S D. 2008. Soil and Agricultural Chemistry Analysis. China Agriculture Press, Beijing. pp. 39–48. (in Chinese)
Benito M, Masaguer A, Moliner A. 2003. Chemical and microbial parameters for the characterization of the stability and maturity of pruning waste compost. Biology and Fertility of Soils, 37, 184–189.
Bernal M P, Alburquerque J A, Moral R. 2009. Composting of animal manures and chemical criteria for compost maturity assessment. A review. Bioresource Technology, 100, 5444–5453.
Bonito G, Isikhuemhen O S, Vilgalys R. 2010. Identification of fungi associated with municipal compost using DNA-based techniques. Bioresource Technology, 101, 1021–1027.
Chroni C, Kyriacou A, Manios T, Lasaridi K E. 2009. Investigation of the microbial community structure and activity as indicators of compost stability and composting process evolution. Bioresource Technology, 100, 3745–3750.
Chung I M, Ahn J K, Yun S J. 2001. Identification of allelopathic compounds from rice (Oryza sativa L.) straw and their biological activity. Canadian Journal of Plant Science, 81, 815–819.
Covino S, Fabianová T, Kresinová Z, Cvancarová M, Burianová E, Filipová A, Vorísková J, Baldrian P, Cajthaml T. 2016. Polycyclic aromatic hydrocarbons degradation and microbial community shifts during co-composting of creosote-treated wood. Journal of Hazardous Materials, 301, 17–26.
Ei F L, Hafidi M, Ouhdouch Y. 2016. Date palm and the activated sludge co-composting actinobacteria sanitization potential. Environmental Technology, 37, 129–135.
Farah Nadia O, Xiang L Y, Lie L Y, Chairil Anuar D, Mohd Afandi M P, Azhari Baharuddin S. 2015. Investigation of physic-chemical properties and microbial community during poultry manure co-composting process. Journal of Environmental Sciences, 28, 81–94.
Garcia C, Hernaandez T, Costa F, Ayuso M. 1992. Evaluation of the maturity of municipal waste compost using simple chemical parameters. Communications in Soil Science and Plant Analysis, 23, 1501–1512.
Gu W J, Lu Y S, Tan Z Y, Xu P Z, Xie K Z, Xia L, Sun L. 2017. Fungi diversity from different depths and time in chicken manure waste static. Bioresource Technology, 239, 447–453.
Haruta S, Cui Z, Huang Z. 2002. Construction of a stable microbial community with high cellulose-degradation ability. Applied Microbiology Biotechnology, 59, 529–534.
Hss S, Lyons G, Chambers J. 2015. Comparison of the changes in mushroom (Agaricus bisporus) compost during windrow and bunker stages of phase I and II. Annals of Applied Biology, 136, 59–68.
Huang H, Huang Y M, Liu X L. 2013. Effect of covering on nitrogen transformation and the quality of pig manure-straw compost. Acta Scientiae Circumstantiae, 33, 780–786. (in Chinese)
Inderjit, Rawat D S, Foy C L. 2004. Multifaceted approach to determine rice straw phytotoxicity. Canadian Journal of Botany, 82, 168–176.
Jiang J, Liu X, Huang Y, Huang H. 2015. Inoculation with nitrogen turnover bacterial agent appropriately increasing nitrogen and promoting maturity in pig manure composting. Waste Management, 39, 78–85. (in Chinese)
Jusoh M L C, Manaf L A, Latiff P A. 2013. Composting of rice straw with effective microorganisms (EM) and its influence on compost quality. Iranian Journal of Environmental Health Sciences and Engineering, 10, 17–17.
Kang W, Kim I, Lee T, Kim K, Kim D. 2014. Effect of temperature on bacterial emissions in composting of swine manure. Waste Management, 34, 1006–1011.
Karadag D, özkaya B, ölmez E, Nissilä M E. 2013. Profiling of bacterial community in a full-scale aerobic composting plant. International Biodeterioration and Biodegradation, 77, 85–90.
Kausar H, Saiah M, Saud H M. 2011. Isolation and screening of potential actinobacteria for rapid composting of rice straw. Biodegradation, 22, 367–375.
Klein M, Brown L, Ashbolt N J, Stuetz R M, Roser D J. 2011. Inactivation of indicators and pathogens in cattle feedlot manures and compost as determined by molecular and culture assays. FEMS Microbiology Ecology, 77, 200–210.
Knerr A, Tripepi R R. 2012. Changes in bacterial communities in dairy manure during nine months of composting as determined by denaturing gradient gel electrophoresis. International Environmental Agreements Politics Law and Economics, 12, 327–342.
Li H, Duan M, Gu J. 2017. Effects of bamboo charcoal on antibiotic resistance genes during chicken manure composting. Ecotoxicology and Environmental Safety, 140, 1–6.
Li K, Bihan M, Yooseph S, Methe B A. 2012. Analyses of the microbial diversity across the human microbiome. PLoS ONE, 7, 32118.
Li Q, Wang X C, Zhang H H, Shi H L, Hu T, Ngo H H. 2013. Characteristics of nitrogen transformation and microbial community in anaerobic composting reactor under two typical temperatures. Bioresource Technology, 137, 270–277.
Li T, Ge X Y, He C N. 2016. Effects of straw retention with mixing maize straw by alfalfa straw or N fertilizer on carbon and nitrogen mineralization and microbial functional diversity. Journal of Agro-Environment Science, 35, 2377–2384. (in Chinese)
Liu C, Dong Y, Hou L, Deng N, Jiao R. 2017. Acidobacteria community responses to nitrogen dose and form in Chinese fir plantations in southern China. Current Microbiology, 74, 396–403.
Liu J, Hai M R, Luo N J. 2014. Effects of different dosing ratio compost materials on cow manure composting process. Chinese Agricultural Science Bulletin, 30, 28–32. (in Chinese)
Liu K S, Rosentrater K A. 2011. Distillers grains: Production, properties, and utilization. New Journal of Physics, 13, 3099–3104.
López-González J A, Suárez-Estrella F, Vargas-García M C. 2015. Dynamics of bacterial microbiota during lignocellulosic waste composting: Studies upon its structure, functionality and biodiversity. Bioresource Technology, 175, 406–416.
Ma J C, Ibekwe A M, Yang C H. 2016. Bacterial diversity and composition in major fresh produce growing soils affected by physio-chemical properties and geographic locations. Science of the Total Environment, 563, 199–209.
Ma X, Huang J, Zhao H L. 2018. Effects of different proportion of straw and nitrogen fertilizer on carbon and nitrogen in red soil microbial biomass. Chinese Journal of Plant Nutrition and Fertilizer, 24, 1574–1580. (in Chinese)
Makan A, Assobhei O, Mountadar, M. 2013. Effect of initial moisture content on the in-vessel composting under air pressure of organic fraction of municipal solid waste in Morocco. Iranian Journal of Environmental Health Science and Engineering, 10, 3–3.
Montserrat A M, August B B. 2008. Evaluation of composting as a strategy for managing organic wastes from a municipal market in Nicaragua. Bioresource Technology, 99, 5120–5124.
Nakhshiniev B, Biddinika M K, Gonzales H B, Sumida H, Yoshikawa K. 2014. Evaluation of hydrothermal treatment in enhancing rice straw compost stability and maturity. Bioresource Technology, 151, 306–313.
Natvig D O, Taylor J W, Tsang A. 2015. Mycothermus thermophilus gen. et comb. nov., a new home for the itinerant thermophile Scytalidium thermophilum (Torula thermophile). Mycologia, 107, 319–327.
Novinscak A, Decoste N J, Surette C. 2009. Characterization of bacterial and fungal communities in composted biosolids over a 2 year period using denaturing gradient gel electrophoresis. Canadian Journal of Microbiology, 55, 375–387.
Paredes C, Cegarra J, Bernal M P. 2005. Influence of olive mill wastewater in composting and impact of the compost on a Swiss chard crop and soil properties. Environment International, 31, 305–312.
Partanen P, Hultman J, Paulin L, Auvinen P, Romantschuk M. 2010. Bacterial diversity at different stages of the composting process. BMC Microbiology, 10, 94–104.
Peters S, Koschinsky S, Schwieger F. 2000. Succession of microbial communities during hot composting as detected by PCR-single-strand-conformation polymorphism-based genetic profiles of small-subunit rRNA genes. Applied and Environmental Microbiology, 66, 930–936.
Raj D, Antil R S. 2011. Evaluation of maturity and stability parameters of composts prepared from agro-industrial wastes. Bioresource Technology, 102, 2868–287.
Rashad F M, Saleh W D, Moselhy M A. 2010. Bioconversion of rice straw and certain agro-industrial wastes to amendments for organic farming systems: 1. Composting, quality, stability and maturity indices. Bioresource Technology, 101, 5952–5960.
Salar R K, Aneja K R. 2007. Thermophilic fungi: Taxonomy and biogeography. Journal of Agricultural Technology, 3, 77–107.
Singh S, Madlala A M, Prior B A. 2003. Thermomyces lanuginosus: Properties of strains and their hemicellulases. FEMS Microbiology Reviews, 27, 3–16.
Sundberg C, Smärs, Jönsson H. 2004. Low pH phase as inhibiting factor in the transition from mesophilic to thermophilic phase in composting. Bioresource Technology, 95, 145–150.
Szekly A J, Sipos R, Berta B. 2009. DGGE and T-RFLP analysis of bacterial succession during mushroom compost production and sequence-aided T-RFLP profile of mature compost. Microbial Ecology, 57, 522–533.
Takaku H, Kodaira S, Kimoto A, Nashimoto M, Takagi M. 2006. Microbial communities in the garbage composting with rice hull as an amendment revealed by culture-dependent and -independent approaches. Journal of Bioscience and Bioengineering, 101, 42–50.
Tian W, Sun Q, Xu D, Zhang Z, Chen D, Li C, Shen Q, Shen B. 2013. Succession of bacterial communities during composting process as detected by 16S rRNA clone libraries analysis. International Biodeterioration and Biodegradation, 78, 58–66.
Tiquia S M, Tam N F. 2002. Characterization and composting of poultry litter in forced-aeration piles. Process Biochemistry, 37, 869–880.
Tkachuk V L, Krause D O, Know N C, Hamm A C, Zvomuya F, Ominski K H, McAllister T A. 2014. Targeted 16S rRNA high-throughput sequencing to characterize microbial communities during composting of livestock mortalities. Journal of Applied Microbiology, 116, 1181–1194.
Tognetti C, Mazzarino M J, Laos F. 2007. Improving the quality of municipal organic waste compost. Bioresource Technology, 98, 1067–1076.
Tumuhairwe J B, Tenywa J S, Otabbong E, Ledin S. 2009. Comparison of four low-technology composting methods for market crop waste. Waste Management, 29, 2274–2281.
Tuomela M. Vikman M, Hatakka A, Itavaava M. 2000. Biodegradation of lignin in a compost environment: A review. Bioresource Technology, 72, 169–183.
Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald G F, Chater K F, Sinderen D. 2007. Genomics of actinobacteria: Tracing the evolutionary history of an ancient phylum. Microbiology and Molecular Biology Reviews, 71, 495–548.
Wang Q Q, Zhou L T, Wang F J. 2018. Application of agricultural waste in green cycle development of agriculture. Journal of Green Science and Technology, 19, 179–182. (in Chinese)
Wang R, Zhang J Y, Sui Q W, Wan H F. 2016. Effect of red mud addition on tetracycline and copper resistance genes and microbial community during the full scale swine manure composting. Bioresource Technology, 216, 1049–1057.
Wang S L, Chen L G, Chen C S. 1994. Cellulase and xylanase production by Aspergillus sp. G-393. Applied Biochemistry and Biotechnology, 45–46, 655.
Wang S Y, Wang Y, Feng X J. 2011. Quantitative analyses of ammonia-oxidizing archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Applied Microbiology and Biotechnology, 90, 779–787. (in Chinese)
Wang X, Selvam A, Chan M. 2013. Nitrogen conservation and acidity control during food wastes composting through struvite formation. Bioresource Technology, 147, 17–22.
Watanabe K, Nagao T T, Kurosawa N. 2009. The dominant bacteria shifted from the order “Lactobacillales” to Bacillales and Actinomycetales during a start-up period of large-scale, completely-mixed composting reactor using plastic bottle flakes as bulking agent. World Journal of Microbiology and Biotechnology, 25, 803–811.
Xiao Y, Zeng G M, Yang Z H, Ma Y H, Huang C, Xu Z Y, Huang J, Fan C Z. 2011. Changes in the actinomycetal communities during continuous thermophilic composting as revealed by denaturing gradient gel electrophoresis and quantitative PCR. Bioresource Technology, 102, 1383–1388.
Xu Z, Mao K M, Tang L. 2005. Effect of microbial strain Rongfeng on the nitrogen dynamic changes in passion fruit marc high-temperature compost process. Journal of Yunnan Agricultural University, 6, 800–803. (in Chinese)
Yuan H Z, Zhu Z K, Wei X M, Liu S L, Peng P Q, Gunina A, Shen J L, Kuzyakov Y, Ge T D, Wu J L, Wang J R. 2019. Straw and biochar strongly affect functional diversity of microbial metabolism in paddy soils. Journal of Integrative Agriculture, 18, 1474–1485.
Zhang M, Li R, Cao L L, Shi J J, Liu H J, Huang Y, Shen Q R. 2014. Algal sludge from Taihu Lake can be utilized to create novel PGPR-containing bio-organic fertilizers. Journal of Environmental Management, 132, 230–236 (in Chinese).
Zhang M, Luo J, Yan S H. 2018. Changes in bacterial communities during two agricultural solid wastes’ co-composting processes. Annals of Microbiology, 68, 743–754. (in Chinese)
Zhang W H, Men M Q, Xu B S. 2018. Dynamic characteristics of the composition of the fungal community in a novel static composting system of dairy manure and rice straw. Journal of Agro-Environment Science, 37, 2029–2036. (in Chinese)
Zhang Y N, Li G X. 2005. Effect of supplementary nitrogen chemical fertilizer on carbon change and degradation of organic pollutants during composting. Journal of Agro-Environment Science, 24, 154–157. (in Chinese)
Zhao R, Lü Y Z, Ma Y B, Li J M. 2020. Effectiveness and longevity of amendments to a cadmium-contaminated soil. Journal of Integrative Agriculture, 19, 1097–1104.
Zhu L, Maruyama J, Kitamoto K. 2013. Further enhanced production of heterologous proteins by double-gene disruption (ΔAosedDΔAovpsl0) in a hyper-producing mutant of Aspergillus oryzae. Applied Microbiology and Biotechnology, 97, 6347–6357. (in Chinese)
Zhu L, Zeng C L, Gao F. 2018. Characteristic analysis of microbial diversity in crud fertilizer from compost of rice straw. Transactions of the Chinese Society of Agricultural Machinery, 49, 228–234. (in Chinese)
Zucconi F, Pera A, Forte M. 1981. Evaluating toxicity of immature compost. Biocycle, 22, 54–57.
[1] CHEN Yun-feng, XIA Xian-ge, HU Cheng, LIU Dong-hai, QIAO Yan, LI Shuang-lai, FAN Xian-peng. Effects of long-term straw incorporation on nematode community composition and metabolic footprint in a rice–wheat cropping system[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2265-2276.
[2] JIN Na, LIU Shi-ming, PENG Huan, HUANG Wen-kun, KONG Ling-an, PENG De-liang. Effect of Aspergillus niger NBC001 on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field[J]. >Journal of Integrative Agriculture, 2021, 20(12): 3230-3239.
[3] CHEN Xue-jiao, LIN Qi-mei, Muhammad Rizwan, ZHAO Xiao-rong, LI Gui-tong. Steam explosion of crop straws improves the characteristics of biochar as a soil amendment[J]. >Journal of Integrative Agriculture, 2019, 18(7): 1486-1495.
[4] LI Wei-hua, LIU Qi-zhi, CHEN Peng. Effect of long-term continuous cropping of strawberry on soil bacterial community structure and diversity[J]. >Journal of Integrative Agriculture, 2018, 17(11): 2570-2582.
[5] YU Zhen-hua, YU Jiang, Makoto Ikenaga, Masao Sakai, LIU Xiao-bing, WANG Guang-hua. Characterization of root-associated bacterial community structures in soybean and corn using locked nucleic acid (LNA) oligonucleotide- PCR clamping and 454 pyrosequencing[J]. >Journal of Integrative Agriculture, 2016, 15(8): 1883-1891.
No Suggested Reading articles found!