厌氧消化过程氨抑制的生物学机理

刘超; 张学萌; 陈闯; 殷玥; 黄海宁; 陈银广

doi:10.13205/j.hjgc.202309019

厌氧消化过程氨抑制的生物学机理

doi: 10.13205/j.hjgc.202309019

同济大学污染控制与资源化研究国家重点实验室, 上海 200092

基金项目:

国家重点研发计划项目（2019YFC1906301）；上海市科委扬帆计划项目（23YF1448900）

详细信息

作者简介:
刘超(1995-),男,博士后,主要研究方向为有机废物生物处理与资源化。chaoliu@tongji.edu.cn

通讯作者:
陈银广(1969-),男,教授,主要研究方向为污染控制与资源化。yinchentj@163.com

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出版历程
- 收稿日期: 2023-07-20
- 网络出版日期: 2023-11-15

BIOLOGICAL MECHANISM OF AMMONIA INHIBITION DURING ANAEROBIC DIGESTION

State Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai 200092, China

摘要

摘要: 厌氧消化作为有机废物无害化处理与能源物质回收的一种有效手段，在实际工程中得以广泛应用。然而厌氧消化过程中产生的高浓度氨氮严重抑制了底物降解和沼气生产，被认为是导致系统性能下降甚至反应体系崩溃的重要因素。厌氧消化的本质是水解酸化菌、产氢产乙酸菌和产甲烷菌等多种微生物利用有机物生产甲烷的过程，故从微生物的角度解析氨抑制机制有助于从源头查明失稳原因，但少有文献对厌氧消化氨抑制的生物学机理进行系统阐述。基于此，首先归纳总结了氨胁迫下微生物菌群结构重塑特征，再着重阐述了高氨氮对细胞关键表型的影响，最后分别探讨了氨抑制下酶和脂质的演变规律，以拓展对厌氧消化氨抑制行为的理解，并提出了氨胁迫下微生物间相互作用和基于氨抑制机理的解抑方法等面向未来的研究方向。
- 厌氧消化 /
- 氨抑制 /
- 菌群结构 /
- 细胞膜 /
- 酶 /
- 脂质 /
- 组学
Abstract: Anaerobic digestion, an effective approach to the harmless treatment of organic waste and recovery of energy and materials, has been widely used in practical engineering. However, the high concentration of ammonia nitrogen produced during anaerobic digestion seriously inhibits substrate degradation and biogas production, which is a vital factor leading to the decline of system performance, and even the collapse of the reaction system. The essence of anaerobic digestion is the process of using organic matter to produce methane by large numbers of microbes, such as hydrolyzing-acidifying and syntrophic acetogenic bacteria and methanogenic archaea. The analysis of the microbial mechanism of ammonia inhibition is conducive to clarifying the essential causes of instability. However, the biological mechanism of ammonia suppression on anaerobic digestion is rarely reviewed. This paper first systematically summarizes the remodeling characteristics of microbial communities under ammonia stress. The influence of high ammonia on the vital phenotypes of cells is then introduced. Finally, the evolution of enzymes and lipid molecules under ammonia stress is discussed. This work will expand the understanding of ammonia inhibition behaviors. Future studies are recommended to reveal the molecular mechanism of microbial interaction under ammonia stress and develop disinhibition methods based on ammonia-inhibiting mechanisms.
- anaerobic digestion /
- ammonia inhibition /
- microflora structure /
- cell membrane /
- enzymes /
- lipids /
- omics

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参考文献(61)

[1]	CALDERON A G, DUAN H, MENG J, et al. An integrated strategy to enhance performance of anaerobic digestion of waste activated sludge[J]. Water Research, 2021, 195:116977.
[2]	SHI Z, CAMPANARO S, USMAN M, et al. Genome-centric metatranscriptomics analysis reveals the role of hydrochar in anaerobic digestion of waste activated sludge[J]. Environmental Science & Technology, 2021, 55(12):8351-8361.
[3]	LI Y, CHEN Z, PENG Y, et al. Deeper insights into the effects of substrate to inoculum ratio selection on the relationship of kinetic parameters, microbial communities, and key metabolic pathways during the anaerobic digestion of food waste[J]. Water Reserach, 2022, 217:118440.
[4]	赵刚, 唐建国, 徐竟成, 等. 中美典型污泥处理处置工程能耗和碳排放比较分析[J]. 环境工程, 2022, 40(12):9-16.
[5]	RAJAGOPAL R, MASSÉ D I, SINGH G. A critical review on inhibition of anaerobic digestion process by excess ammonia[J]. Bioresource Technology, 2013, 143:632-641.
[6]	JIANG Y, MCADAM E, ZHANG Y, et al. Ammonia inhibition and toxicity in anaerobic digestion:a critical review[J]. Journal of Water Process Engineering, 2019, 32:100899.
[7]	WANG Z, JIANG Y, WANG S, et al. Impact of total solids content on anaerobic co-digestion of pig manure and food waste:insights into shifting of the methanogenic pathway[J]. Waste Management, 2020, 114:96-106.
[8]	何仕均, 王建龙, 赵璇. 氨氮对厌氧颗粒污泥产甲烷活性的影响[J]. 清华大学学报(自然科学版), 2005, 9(45):1294-1296.
[9]	LIU C, HUANG H, DUAN X, et al. Integrated metagenomic and metaproteomic analyses unravel ammonia toxicity to active methanogens and syntrophs, enzyme synthesis, and key enzymes in anaerobic digestion[J]. Environmental Science & Technology, 2021, 55(21):14817-14827.
[10]	ZHANG H, YUAN W, DONG Q, et al. Integrated multi-omics analyses reveal the key microbial phylotypes affecting anaerobic digestion performance under ammonia stress[J]. Water Research, 2022, 213:118152.
[11]	LIU Y, NGO H H, GUO W, et al. The roles of free ammonia (FA) in biological wastewater treatment processes:a review[J]. Environment International, 2019, 123:10-19.
[12]	SAHA S, BASAK B, HWANG J H, et al. Microbial symbiosis:a network towards biomethanation[J]. Trends in Microbiology, 2020, 28(12):968-984.
[13]	CARBALLA M, REGUEIRO L, LEMA J M. Microbial management of anaerobic digestion:exploiting the microbiome-functionality nexus[J]. Current Opinion in Biotechnology, 2015, 33:103-111.
[14]	SIEBER J R, MCINERNEY M J, GUNSALUS R P. Genomic insights into syntrophy:the paradigm for anaerobic metabolic cooperation[J]. Annual Review of Microbiology, 2012, 66:429-452.
[15]	SPROTT G D, PATEL G B. Ammonia toxicity in pure cultures of methanogenic bacteria[J]. Systematic and Applied Microbiology, 1986, 7(2/3):358-363.
[16]	FOTIDIS I A, KARAKASHEV D, ANGELIDAKI I. The dominant acetate degradation pathway/methanogenic composition in full-scale anaerobic digesters operating under different ammonia levels[J]. International Journal of Environmental Science and Technology, 2013, 11(7):2087-2094.
[17]	WANG Z, WANG S, HU Y, et al. Distinguishing responses of acetoclastic and hydrogenotrophic methanogens to ammonia stress in mesophilic mixed cultures[J]. Water Research, 2022, 224:119029.
[18]	LV Z, LEITE A F, HARMS H, et al. Microbial community shifts in biogas reactors upon complete or partial ammonia inhibition[J]. Applied Microbiology and Biotechnology, 2019, 103(1):519-533.
[19]	RUIZ-SANCHEZ J, CAMPANARO S, GUIVERNAU M, et al. Effect of ammonia on the active microbiome and metagenome from stable full-cale digesters[J]. Bioresource Technology, 2018, 250:513-522.
[20]	CHEN H, WANG W, XUE L, et al. Effects of ammonia on anaerobic digestion of food waste:process performance and microbial community[J]. Energy & Fuels, 2016, 30(7):5749-5757.
[21]	CHRISTOU M L, VASILEIADIS S, KALAMARAS S D, et al. Ammonia-induced inhibition of manure-based continuous biomethanation process under different organic loading rates and associated microbial community dynamics[J]. Bioresource Technology, 2021, 320:124323.
[22]	HE L, YU J, LIN Z, et al. Organic matter removal performance, pathway and microbial community succession during the construction of high-ammonia anaerobic biosystems treating anaerobic digestate food waste effluent[J]. Journal of Environmental Management, 2022, 317:115428.
[23]	彭韵, 李蕾, 伍迪, 等. 微生物群落对氨胁迫响应的宏基因组学研究[J]. 中国环境科学, 2022, 42(2):777-786.
[24]	CALLI B, MERTOGLU B, INANC B, et al. Effects of high free ammonia concentrations on the performances of anaerobic bioreactors[J]. Process Biochemistry, 2005, 40(3/4):1285-1292.
[25]	ZHANG C, YUAN Q, LU Y. Inhibitory effects of ammonia on syntrophic propionate oxidation in anaerobic digester sludge[J]. Water Research, 2018, 146:275-287.
[26]	PENG X, ZHANG S, LI L, et al. Long-term high-solids anaerobic digestion of food waste:effects of ammonia on process performance and microbial community[J]. Bioresource Technology, 2018, 262:148-158.
[27]	ZHANG H, PENG Y, YANG P, et al. Response of process performance and microbial community to ammonia stress in series batch experiments[J]. Bioresource Technology, 2020, 314:123768.
[28]	YE M, ZHU A, SUN B, et al. Methanogenic treatment of dairy product wastewater by thermophilic anaerobic membrane bioreactor:ammonia inhibition and microbial community[J]. Bioresource Technology, 2022, 357:127349.
[29]	MLINAR S, WEIG A R, FREITAG R. Influence of NH₃ and NH₄⁺ on anaerobic digestion and microbial population structure at increasing total ammonia nitrogen concentrations[J]. Bioresource Technology, 2022, 361:127638.
[30]	CYPIONKA H, WIDDEL F, PFENNIG N. Survival of sulfate-reducing bacteria after oxygen stress, and growth in sulfate-free oxygen-sulfide gradients[J]. FEMS microbiology ecology, 1985, 1(1):39-45.
[31]	BOONE D R, BRYANT M P. Propionate-degrading bacterium, Syntrophobacter wolinii sp. nov. gen. nov., from methanogenic ecosystems[J]. Applied and Environmental Microbiology, 1980, 40(3):626-632.
[32]	DWYER D F, WEEG-AERSSENS E, SHELTON D R, et al. Bioenergetic conditions of butyrate metabolism by a syntrophic, anaerobic bacterium in coculture with hydrogen-oxidizing methanogenic and sulfidogenic bacteria[J]. Applied and Environmental Microbiology, 1988, 54(6):1354-1359.
[33]	LIU C, ZHANG X, CHEN C, et al. Physiological responses of Methanosarcina barkeri under ammonia stress at the molecular level:the unignorable lipid reprogramming[J]. Environmental Science & Technology, 2023, 57(9):3917-3929.
[34]	MCNEIL P L, STEINHARDT R A. Loss, restoration, and maintenance of plasma membrane integrity[J]. The Journal of Cell Biology, 1997, 137(1):1-4.
[35]	CALLI B, MERTOGLU B, INANC B, et al. Methanogenic diversity in anaerobic bioreactors under extremely high ammonia levels[J]. Enzyme and Microbial Technology, 2005, 37(4):448-455.
[36]	CALLI B, MERTOGLU B, INANC B, et al. Community changes during start-up in methanogenic bioreactors exposed to increasing levels of ammonia[J]. Environmental Technology, 2005, 26(1):85-91.
[37]	JEYENDRAN R, VAN DER VEN H, PEREZ-PELAEZ M, et al. Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics[J]. Reproduction, 1984, 70(1):219-228.
[38]	ROY S, MONDAL A, YADAV V, et al. Mechanistic insight into the antibacterial activity of chitosan exfoliated MoS₂ nanosheets:membrane damage, metabolic inactivation, and oxidative stress[J]. ACS Applied Bio Materials, 2019, 2(7):2738-2755.
[39]	SCHNAIDER L, BRAHMACHARI S, SCHMIDT N W, et al. Self-assembling dipeptide antibacterial nanostructures with membrane disrupting activity[J]. Nature Communication, 2017, 8(1):1365.
[40]	PENG Y, LI L, YANG P, et al. Integrated genome-centric metagenomic and metaproteomic analyses unravel the responses of the microbial community to ammonia stress[J]. Water Research, 2023, 242:120239.
[41]	PADMAKUMAR R, PADMAKUMAR R, BANERJEE R. Evidence that cobalt-carbon bond homolysis is coupled to hydrogen atom abstraction from substrate in methylmalonyl-CoA mutase[J]. Biochemistry, 1997, 36(12):3713-3718.
[42]	WEBSTER M W, TAKACS M, ZHU C, et al. Structural basis of transcription-translation coupling and collision in bacteria[J]. Science, 2020, 369(6509):1355-1359.
[43]	KORKHIN Y, UNLIGIL U M, LITTLEFIELD O, et al. Evolution of complex RNA polymerases:the complete archaeal RNA polymerase structure[J]. PLoS Biology, 2009, 7(5):e1000102.
[44]	YUSUPOV M M, YUSUPOVA G Z, BAUCOM A, et al. Crystal structure of the ribosome at 5.5Å resolution[J]. Science, 2001, 292(5518):883-896.
[45]	SCHMEING T M, VOORHEES R M, KELLEY A C, et al. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA[J]. Science, 2009, 326(5953):688-694.
[46]	KAYHANIAN M. Ammonia inhibition in high-solids biogasification:an overview and practical solutions[J]. Environmental Technology, 1999, 20(4):355-365.
[47]	FERREIRA T, CARRONDO M, ALVES P. Effect of ammonia production on intracellular pH:consequent effect on adenovirus vector production[J]. Journal of Biotechnology, 2007, 129(3):433-438.
[48]	SPROTT G D, SHAW K M, JARRELL K F. Ammonia/potassium exchange in methanogenic bacteria[J]. Journal of Biological Chemistry, 1984, 259(20):12602-12608.
[49]	WITTMANN C, ZENG A P, DECKWER W D. Growth inhibition by ammonia and use of a pH-controlled feeding strategy for the effective cultivation of Mycobacterium chlorophenolicum[J]. Applied Microbiology and Biotechnology, 1995, 44(3):519-525.
[50]	KUHNER C, DRAKE H, ALM E, et al. Methane production and oxidation by soils from acidic forest wetlands of east-central Germany[C]//Abstr 96th Gen Meet Am Soc Microbiol American Society for Microbiology. Washington, DC, 1996:304.
[51]	LLOYD C T, IWIG D F, WANG B, et al. Discovery, structure and mechanism of a tetraether lipid synthase[J]. Nature, 2022, 609(7925):197-203.
[52]	HARAYAMA T, RIEZMAN H. Understanding the diversity of membrane lipid composition[J]. Nature Reviews Molecular Cell Biology, 2018, 19(5):281-296.
[53]	LOPEZ-LARA I M, GEIGER O. Bacterial lipid diversity[J]. Biochimica et biophysica acta:molecular and cell biology of lipids, 2017, 1862(11):1287-1299.
[54]	QI Z, SUN N, LIU C. Glyoxylate cycle maintains the metabolic homeostasis of Pseudomonas aeruginosa in viable but nonculturable state induced by chlorine stress[J]. Microbiological Research, 2023, 270:127341.
[55]	BALLWEG S, SEZGIN E, DOKTOROVA M, et al. Regulation of lipid saturation without sensing membrane fluidity[J]. Nature Communinations, 2020, 11(1):756.
[56]	LI R, GUINEY L M, CHANG C H, et al. Surface oxidation of graphene oxide determines membrane damage, lipid peroxidation, and cytotoxicity in macrophages in a pulmonary toxicity model[J]. ACS Nano, 2018, 12(2):1390-1402.
[57]	SHANTA P V, LI B, STUART D D, et al. Lipidomic profiling of algae with microarray MALDI-MS toward ecotoxicological monitoring of herbicide exposure[J]. Environmental Science & Technology, 2021, 55(15):10558-10568.
[58]	MARQUENO A, BLANCO M, MACEDA-VEIGA A, et al. Skeletal muscle lipidomics as a new tool to determine altered lipid homeostasis in fish exposed to urban and industrial wastewaters[J]. Environmental Science Technology, 2019, 53(14):8416-8425.
[59]	TANIGUCHI M, OKAZAKI T. The role of sphingomyelin and sphingomyelin synthases in cell death, proliferation and migration-from cell and animal models to human disorders[J]. Biochimica Biophysica Acta, Mol. Cell Biology Lipids, 2014, 1841(5):692-703.
[60]	TANIGUCHI M, OKAZAKI T. Role of ceramide/sphingomyelin (SM) balance regulated through "SM cycle" in cancer[J]. Cell Signalling, 2021, 87:110119.
[61]	YANG P, PENG Y, LIU H, et al. Multi-scale analysis of the foaming mechanism in anaerobic digestion of food waste:from physicochemical parameter, microbial community to metabolite response[J]. Water Research, 2022, 218:118482.