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Synergy effects of Methylomonas koyamae and Hyphomicrobium methylovorum under methanethiol stress

  • Environmental Biotechnology
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Abstract   

Methanotrophs are able to metabolize volatile organic sulfur compounds (VOSCs), excrete organic carbon during CH4 oxidation, and influence microbial community structure and function of the ecosystem. In return, microbial community structure and environmental factors can affect the growth metabolism of methanotrophs. In this study, Methylomonas koyamae and Hyphomicrobium methylovorum were used for model organisms, and methanethiol (MT) was chosen for a typical VOSC to investigate the synergy effects under VOSC stress. The results showed that when Hyphomicrobium methylovorum was co-cultured with Methylomonas koyamae in the medium with CH4 used as the carbon source, the co-culture had better MT tolerance relative to Methylomonas koyamae and oxidized all CH4 within 120 h, even at the initial MT concentration of 2000 mg m−3. The optimal co-culture ratios of Methylomonas koyamae to Hyphomicrobium methylovorum were 4:1–12:1. Although MT could be converted spontaneously to dimethyl disulfide (DMDS), H2S, and CS2 in air, faster losses of MT, DMDS, H2S, and CS2 were observed in each strain mono-culture and the co-culture. Compared with Hyphomicrobium methylovorum, MT was degraded more quickly in the Methylomonas koyamae culture. During the co-culture, the CH4 oxidation process of Methylomonas koyamae could provide carbon and energy sources for the growth of Hyphomicrobium methylovorum, while Hyphomicrobium methylovorum oxidized MT to help Methylomonas koyamae detoxify. These findings are helpful to understand the synergy effects of Methylomonas koyamae and Hyphomicrobium methylovorum under MT stress and enrich the role of methanotrophs in the sulfur biogeochemical cycle.

Key points

• The co-culture of Methylomonas and Hyphomicrobium has better tolerance to CH 3 SH.

• Methylomonas can provide carbon sources for the growth of Hyphomicrobium.

• The co-culture of Methylomonas and Hyphomicrobium enhances the removal of CH 4 and CH 3 SH.

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Data availability statement

The original contributions presented in the study are included in the article. Further inquiries can be directed to the corresponding author.

References   

  • Benassi R (2004) Ab initio study of the oxidation of CH3SH to CH3SSCH3. Theor Chem Acc 112(2):95–105

    Article  CAS  Google Scholar 

  • Bodelier PLE, Meima-Franke M, Hordijk CA, Steenbergh AK, Hefting M, Bodrossy L, Mv B, Seifert J (2013) Microbial minorities modulate methane consumption through niche partitioning. ISME J 7:2214–2228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boden R, Kelly DP, Murrell JC, Schäfer H (2010) Oxidation of dimethylsulfide to tetrathionate by Methylophaga thiooxidans sp. nov.: a new link in the sulfur cycle. Environ Microbiol 12(10):2688–2699

    CAS  PubMed  Google Scholar 

  • Cáceres M, Morales M, Martín RS, Urrutia H, Aroca G (2010) Oxidation of volatile reduced sulphur compounds in biotrickling filter inoculated with Thiobacillus thioparus. Electron J Biotechnol 13(5):1–11

    Article  Google Scholar 

  • Chen M, Yao X, Ma R, Song Q, Long Y, He R (2017) Methanethiol generation potential from anaerobic degradation of municipal solid waste in landfills. Environ Sci Pollut Res 24(30):23992–24001

    Article  CAS  Google Scholar 

  • Cho K-s, Hirai M, Shoda M (1992) Enhanced removability of odorous sulfur-containing gases by mixed cultures of purified bacteria from peat biofilters. J Ferment Bioeng 73:219–224

    Article  Google Scholar 

  • de Zwart JMM, Nelisse PN, Kuenen JG (1996) Isolation and characterization of Methylophaga sulfidovorans sp. nov.: an obligately methylotrophic, aerobic, dimethylsulfide oxidizing bacterium from a microbial mat. FEMS Microbiol Ecol 20(4):261–270

    Article  Google Scholar 

  • Eyice Ö, Myronova N, Pol A, Carrión O, Todd JD, Smith TJ, Gurman SJ, Cuthbertson A, Mazard S, Mennink-Kersten MASH, Bugg TDH, Andersson KK, Johnston AWB, Op den Camp HJM, Schäfer H (2018) Bacterial SBP56 identified as a Cu-dependent methanethiol oxidase widely distributed in the biosphere. ISME J 12(1):145–160

    Article  CAS  PubMed  Google Scholar 

  • Fernandez HT, Rico IR, Prida JJdl, Langenhove HV (2013) Dimethyl sulfide bioflltration using immobilized Hyphomicrobium VS and Thiobadllus thioparus TK-m in sugarcane bagasse. Environ Technol 34(2):257–262

    Article  CAS  Google Scholar 

  • Fernández HTT, Rico ILR, de la Prida JJ, Van Langenhove HR (2013) Dimethyl sulfide biofiltration using immobilized Hyphomicrobium VS and Thiobacillus thioparus TK-m in sugarcane bagasse. Environ Technol 34(2):257–262

    Article  Google Scholar 

  • Gęsicka A, Oleskowicz-Popiel P, Łężyk M (2021) Recent trends in methane to bioproduct conversion by methanotrophs. Biotechnol Adv 53:107861

    Article  PubMed  Google Scholar 

  • Gu W, Sun W, Lu Y, Li X, Xu P, **e K, Sun L, Wu H (2018) Effect of Thiobacillus thioparus 1904 and sulphur addition on odour emission during aerobic composting. Bioresour Technol 249:254–260

    Article  CAS  PubMed  Google Scholar 

  • Gwak J-H, Awala SI, Nguyen N-L, Yu W-J, Yang H-Y, von Bergen M, Jehmlich N, Kits KD, Loy A, Dunfield PF, Dahl C, Hyun J-H, Rhee S-K (2022) Sulfur and methane oxidation by a single microorganism. Proc Natl Acad Sci USA 119(32):e2114799119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He R, **a F, Bai Y, Wang J, Shen D (2012) Mechanism of H2S removal during landfill stabilization in waste biocover soil, an alterative landfill cover. J Hazard Mater 217–218:67–75

    Article  PubMed  Google Scholar 

  • He R, Yao X, Chen M, Ma R, Li H, Wang C, Ding S (2018) Conversion of sulfur compounds and microbial community in anaerobic treatment of fish and pork waste. Waste Manage 76:383–393

    Article  CAS  Google Scholar 

  • He R, Su Y, Leewis MC, Chu Y, Wang J, Ma R, Wu D, Zhan L, Herriott IC, Leigh MB (2020) Low O2 level enhances CH4-derived carbon flow into microbial communities in landfill cover soils. Environ Pollut 258:113676

    Article  CAS  PubMed  Google Scholar 

  • He R, Wang J, Pohlman JW, Jia Z, Chu Y, Wooller MJ, Leigh MB (2022) Metabolic flexibility of aerobic methanotrophs under anoxic conditions in Arctic lake sediments. ISME J 16:78–90

    Article  CAS  PubMed  Google Scholar 

  • Jia T, Sun S, Chen K, Zhang L, Peng Y (2020) Simultaneous methanethiol and dimethyl sulfide removal in a single-stage biotrickling filter packed with polyurethane foam: performance, parameters and microbial community analysis. Chemosphere 244:125460

    Article  CAS  PubMed  Google Scholar 

  • Kalyuzhnaya MG, Yang S, Rozova ON, Smalley NE, Clubb J, Lamb AD, Gowda GAN, Raftery D, Fu Y, Fo B, Vuilleumier S, Beck DAC, Trotsenko YA, Khmelenina VN, Lidstrom ME (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4:2785

    Article  CAS  PubMed  Google Scholar 

  • Kim Hg, Doronina NV, Trotsenko YA, Kim SW (2007) Methylophaga aminisulfidivorans sp. nov., a restricted facultatively methylotrophic marine bacterium. Int J Syst Evol Microbiol 57(9):2096–2101

  • Krober E, Schafer H (2019) Identification of proteins and genes expressed by Methylophaga thiooxydans during growth on dimethylsulfide and their presence in other members of the genus. Front Microbiol 10:1132

    Article  PubMed  PubMed Central  Google Scholar 

  • Ksibi M (2006) Chemical oxidation with hydrogen peroxide for domestic wastewater treatment. Chem Eng J 119(2–3):161–165

    Article  CAS  Google Scholar 

  • Lee C-L, Brimblecombe P (2016) Anthropogenic contributions to global carbonyl sulfide, carbon disulfide and organosulfides fluxes. Earth-Sci Rev 160:1–18

    Article  CAS  Google Scholar 

  • Lee SG, Goo JH, Kim HG, Oh J-I, Kim YM, Kim SW (2004) Optimization of methanol biosynthesis from methane using Methylosinus trichosporium OB3b. Biotechnol Lett 26:947–950

    Article  CAS  PubMed  Google Scholar 

  • Lee J-H, Kim TG, Cho K-S (2012) Isolation and characterization of a facultative methanotroph degrading malodor-causing volatile sulfur compounds. J Hazard Mater 235–236:224–229

    Article  PubMed  Google Scholar 

  • Li Y, Gong X, Zhao Z, Shen Q, Zhang L (2022) Distribution and release of volatile organic sulfur compounds in Yangcheng Lake. Water 14:1199

    Article  CAS  Google Scholar 

  • Ma R-C, Chu Y-X, Wang J, Wang C, Leigh MB, Chen Y, He R (2021) Stable-isotopic and metagenomic analyses reveal metabolic and microbial link of aerobic methane oxidation coupled to denitrification at different O2 levels. Sci Total Environ 764:142901

    Article  CAS  PubMed  Google Scholar 

  • Manheim DC, Yeşiller N, Hanson JL (2021) Climate change effects of gases from municipal solid waste landfills. Jpn Geotech Soc Spec Publ 9(4):142–147

    Google Scholar 

  • Oshkin IY, Beck DAC, Lamb AE, Tchesnokova V, Benuska G, McTaggart TL, Kalyuzhnaya MG, Dedysh SN, Lidstrom ME, Chistoserdova L (2014) Methane-fed microbial microcosms show differential community dynamics and pinpoint taxa involved in communal response. ISME J 9:1119–1129

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozbay G, Jones MB, Gadde M, Isah S, Attarwala T (2021) Design and operation of effective landfills with minimal effects on the environment and human health. J Environ Public Health 2021:6921607

    Article  PubMed  PubMed Central  Google Scholar 

  • Pokorna D, Zabranska J (2015) Sulfur-oxidizing bacteria in environmental technology. Biotechnol Adv 33(6):1246–1259

    Article  CAS  PubMed  Google Scholar 

  • Prenafeta-Boldú FX, Rojo N, Gallastegui G, Guivernau M, Viñas M, Elias A (2014) Role of Thiobacillus thioparus in the biodegradation of carbon disulfide in a biofilter packed with a recycled organic pelletized material. Biodegradation 25:557–568

    Article  PubMed  Google Scholar 

  • Rahalkar MC (2006) Aerobic methanotrophic bacterial communities in sediments of Lake Constance.

  • Rojo N, Gallastegi G, Barona A, Gurtubay L, Ibarra-Berastegi G, Elias A (2010) Biotechnology as an alternative for carbon disulfide treatment in air pollution control. Environ Rev 18:321–332

    Article  CAS  Google Scholar 

  • Schiffman SS, Bennett JL, Raymer JH (2001) Quantification of odors and odorants from swine operations in North Carolina. Agric for Meteorol 108(3):213–240

    Article  Google Scholar 

  • Schmitz RA, Peeters SH, Versantvoort W, Picone N, Pol A, Jetten MSM, Op den Camp HJM (2021) Verrucomicrobial methanotrophs: ecophysiology of metabolically versatile acidophiles. FEMS Microbiol Rev 45(5):007

    Article  Google Scholar 

  • Schmitz RA, Mohammadi SS, van Erven T, Berben T, Jetten MSM, Pol A, Op den Camp HJM (2022) Methanethiol consumption and hydrogen sulfide production by the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV. Front Microbiol 13:857442

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmitz RA, Peeters SH, Mohammadi SS, Berben T, van Erven T, Iosif CA, van Alen T, Versantvoort W, Jetten MSM, Op den Camp HJM, Pol A (2022b) Methanotrophs are vigorous H2S oxidizers using a sulfide:quinone oxidoreductase and a ba3-type terminal oxidase. bioRxiv:505896. https://doi.org/10.1101/2022.08.31.505896

  • Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34(4):496–531

    Article  CAS  PubMed  Google Scholar 

  • Shihab MS, Mhemid RKS, Saeed L, Ismail H, Alp K (2022) Reducing volatile organic compound emissions using biotrickling filters and bioscrubber systems. J Ecol Eng 23(10):255–268

    Article  Google Scholar 

  • Shmareva MN, Doronina NV, Tarlachkov SV, Vasilenko OV, Trotsenko YA (2018) Methylophaga muralis Bur 1, a haloalkaliphilic methylotroph isolated from the Khilganta soda lake (Southern Transbaikalia, Buryat Republic). Microbiology 87:33–46

    Article  CAS  Google Scholar 

  • Siddharth T, Sridhar P, Vinila VS, Tyagi RD (2021) Environmental applications of microbial extracellular polymeric substance (EPS): a review. J Environ Manage 287:112307

    Article  CAS  PubMed  Google Scholar 

  • Sonawane JM, Rai AK, Sharma M, Tripathi M, Prasad R (2022) Microbial biofilms: recent advances and progress in environmental bioremediation. Sci Total Environ 824:153843

    Article  CAS  PubMed  Google Scholar 

  • Su Y, Zhang X, Wei X, Kong J, **a F, Li W, He R (2014) Evaluation of simultaneous biodegradation of methane and toluene in landfill covers. J Hazard Mater 274:367–375

    Article  CAS  PubMed  Google Scholar 

  • Suylen G, Large PJ, Dijken J, Kuenen JG (1987) Methyl mercaptan oxidase, a key enzyme in the metabolism of methylated sulphur compounds by Hyphomicrobium EG. J Gen Microbiol 133(11):2989–2997

    CAS  Google Scholar 

  • Tilmes S, Muller R, Salawitch RJ, Schmidt U, Webster CR, Oelhaf H, Camy-Peyret C, Russell JM (2008) Chemical ozone loss in the Arctic winter 1991–1992. Copernicus GmbH 8(7):1897–1910

    CAS  Google Scholar 

  • van Spanning RJM, Guan Q, Melkonian C, Gallant JL, Polerecky L, Flot JF, Brandt BW, Braster M, Iturbe Espinoza P, Aerts JW, Meima-Franke M, Piersma SR, Bunduc CM, Ummels R, Pain A, Fleming EJ, van der Wel NN, Gherman VD, Sarbu SM, Bodelier PLE, Bitter W (2022) Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem. Nat Microbiol 7:2089–2100

    Article  PubMed  Google Scholar 

  • Wang J, **a F, Bai Y, Fang C, Shen D, He R (2011) Methane oxidation in landfill waste biocover soil: kinetics and sensitivity to ambient conditions. Waste Manage 31(5):864–870

    Article  CAS  Google Scholar 

  • Wang J, Chu Y, Yao X, He R (2021) Enhanced degradation of methanethiol in enrichment cultures in the presence of methane. Biochem Eng J 168:107934

    Article  CAS  Google Scholar 

  • Wang J, Wei Z, Chu Y-X, Tian G-M, He R (2022) Eutrophic levels and algae growth increase emissions of methane and volatile sulfur compounds from lakes. Environ Pollut 306:119435

    Article  CAS  PubMed  Google Scholar 

  • Watson SB, Jüttner F (2017) Malodorous volatile organic sulfur compounds: sources, sinks and significance in inland waters. Crit Rev Microbiol 43(2):210–237

    Article  CAS  PubMed  Google Scholar 

  • Wei Z, Sun J, JC H, Huang Q, Chen Z, Ye Q, Luo Y (2014) Dimethyl sulfide removal using biofilter immobilized Thiobacillus sp. ST22. J Environ Eng 140(11):06014004

    Article  CAS  Google Scholar 

  • Wei X, Su Y, Zhang H, Chen M, He R (2015) Responses of methanotrophic activity, community and EPS production to CH4 and O2 concentrations in waste biocover soils. Waste Manage 42:118–127

    Article  Google Scholar 

  • Yang H, Jung H, Oh K-C, Jeon J-M, Cho K-S (2021) Characterization of the bacterial community associated with methane and odor in a pilot-scale landfill biocover under moderately thermophilic conditions. J Microbiol Biotechnol 31(6):803–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao X, Ma R, Li H, Wang C, Zhang C, Yin S, Wu D, He X, Wang J, Zhan L, He R (2019) Assessment of the major odor contributors and health risks of volatile compounds in three disposal technologies for municipal solid waste. Waste Manage 91:128–138

    Article  CAS  Google Scholar 

  • Zhang L, Hirai M, Shoda M (1991) Removal characteristics of dimethyl sulfide, methanethiol and hydrogen sulfide by Hyphomicrobium sp. 155 isolated from peat biofilter. J Ferment Bioeng 72:392–396

    Article  CAS  Google Scholar 

  • Zhou J, Zheng G, Wong JWC, Zhou L (2013) Degradation of inhibitory substances in sludge by Galactomyces sp. Z3 and the role of its extracellular polymeric substances in improving bioleaching. Bioresour Technol 132:217–223

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Xu X, Yuan M, Wu H, Ma Z, Wu W (2017) Optimum O2:CH4 ratio promotes the synergy between aerobic methanotrophs and denitrifiers to enhance nitrogen removal. Front Microbiol 8:1112

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was financially supported by the Natural Science Foundation of Zhejiang Province with Grant No. LZ20E080002, the National Natural Science Foundation of China with Grant Nos. 91851109 and 41911530193, and the Central Guide Local Science and Technology Development of **njiang Uygur Autonomous Region with Grant No. ZYYD2023B16.

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XZ performed the experiments and wrote the manuscript. HJL, LJ, and JW performed the experiments and analyzed the data. RH conceived the project and wrote the manuscript.

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Correspondence to Ruo He.

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Zhang, X., Li, HJ., Jiang, L. et al. Synergy effects of Methylomonas koyamae and Hyphomicrobium methylovorum under methanethiol stress. Appl Microbiol Biotechnol 107, 3099–3111 (2023). https://doi.org/10.1007/s00253-023-12472-w

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