Co-cultured Methanogen Improved the Metabolism in the Hydrogenosome of Anaerobic Fungus As Revealed by Gas Chromatography-mass Spectrometry Analysis

Overview

Journal Asian-Australas J Anim Sci

Specialty Veterinary Medicine

Date 2020 Feb 15

PMID 32054157

Citations 5

Authors

Yuqi Li

Meizhou Sun

Yuanfei Li

Yanfen Cheng

Weiyun Zhu

Affiliations

Soon will be listed here.

Abstract

Objective: The purpose of this study was to reveal the metabolic shift in the fungus cocultured with the methanogen (Methanobrevibacter thaueri).

Methods: Gas chromatography-mass spectrometry was used to investigate the metabolites in anaerobic fungal (Pecoramyces sp. F1) cells and the supernatant.

Results: A total of 104 and 102 metabolites were detected in the fungal cells and the supernatant, respectively. The partial least squares-discriminant analysis showed that the metabolite profiles in both the fungal cell and the supernatant were distinctly shifted when co-cultured with methanogen. Statistically, 16 and 30 metabolites were significantly (p<0.05) affected in the fungal cell and the supernatant, respectively by the co-cultured methanogen. Metabolic pathway analysis showed that co-culturing with methanogen reduced the production of lactate from pyruvate in the cytosol and increased metabolism in the hydrogenosomes of the anaerobic fungus. Citrate was accumulated in the cytosol of the fungus co-cultured with the methanogen.

Conclusion: The co-culture of the anaerobic fungus and the methanogen is a good model for studying the microbial interaction between H2-producing and H2-utilizing microorganisms. However, metabolism in hydrogenosome needs to be further studied to gain better insight in the hydrogen transfer among microorganisms.

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References

Akhmanova A, Voncken F, Hosea K, Harhangi H, Keltjens J, Op den Camp H . A hydrogenosome with pyruvate formate-lyase: anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol Microbiol. 1999; 32(5):1103-14. DOI: 10.1046/j.1365-2958.1999.01434.x. View

Sun M, Jin W, Li Y, Mao S, Cheng Y, Zhu W . [Isolation and identification of cellulolytic anaerobic fungi and their associated methanogens from holstein cow]. Wei Sheng Wu Xue Bao. 2014; 54(5):563-71. View

Bauchop T, Mountfort D . Cellulose fermentation by a rumen anaerobic fungus in both the absence and the presence of rumen methanogens. Appl Environ Microbiol. 1981; 42(6):1103-10. PMC: 244160. DOI: 10.1128/aem.42.6.1103-1110.1981. View

Orpin C . Studies on the rumen flagellate Neocallimastix frontalis. J Gen Microbiol. 1975; 91(2):249-62. DOI: 10.1099/00221287-91-2-249. View

Marvin-Sikkema F, Pedro Gomes T, Grivet J, Gottschal J, Prins R . Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch Microbiol. 1993; 160(5):388-96. DOI: 10.1007/BF00252226. View

Haitjema C, Solomon K, Henske J, Theodorou M, OMalley M . Anaerobic gut fungi: Advances in isolation, culture, and cellulolytic enzyme discovery for biofuel production. Biotechnol Bioeng. 2014; 111(8):1471-82. DOI: 10.1002/bit.25264. View

Edwards J, Forster R, Callaghan T, Dollhofer V, Dagar S, Cheng Y . PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities. Front Microbiol. 2017; 8:1657. PMC: 5622200. DOI: 10.3389/fmicb.2017.01657. View

Barichievich E, Calza R . Supernatant protein and cellulase activities of the anaerobic ruminal fungus Neocallimastix frontalis EB188. Appl Environ Microbiol. 1990; 56(1):43-8. PMC: 183248. DOI: 10.1128/aem.56.1.43-48.1990. View

Cheng Y, Jin W, Mao S, Zhu W . Production of Citrate by Anaerobic Fungi in the Presence of Co-culture Methanogens as Revealed by (1)H NMR Spectrometry. Asian-Australas J Anim Sci. 2014; 26(10):1416-23. PMC: 4093067. DOI: 10.5713/ajas.2013.13134. View

10.

Wei Y, Long R, Yang H, Yang H, Shen X, Shi R . Fiber degradation potential of natural co-cultures of Neocallimastix frontalis and Methanobrevibacter ruminantium isolated from yaks (Bos grunniens) grazing on the Qinghai Tibetan Plateau. Anaerobe. 2016; 39:158-64. DOI: 10.1016/j.anaerobe.2016.03.005. View

11.

Jin W, Cheng Y, Mao S, Zhu W . Isolation of natural cultures of anaerobic fungi and indigenously associated methanogens from herbivores and their bioconversion of lignocellulosic materials to methane. Bioresour Technol. 2011; 102(17):7925-31. DOI: 10.1016/j.biortech.2011.06.026. View

12.

Teunissen M, Kets E, Op den Camp H, Huis Int Veld J, Vogels G . Effect of coculture of anaerobic fungi isolated from ruminants and non-ruminants with methanogenic bacteria on cellulolytic and xylanolytic enzyme activities. Arch Microbiol. 1992; 157(2):176-82. DOI: 10.1007/BF00245287. View

13.

Wei Y, Yang H, Luan Y, Long R, Wu Y, Wang Z . Isolation, identification and fibrolytic characteristics of rumen fungi grown with indigenous methanogen from yaks (Bos grunniens) grazing on the Qinghai-Tibetan Plateau. J Appl Microbiol. 2016; 120(3):571-87. DOI: 10.1111/jam.13035. View

14.

Ma B, Li X, Zhang Q, Wu D, Wang G, A J . Metabonomic profiling in studying anti-osteoporosis effects of strontium fructose 1,6-diphosphate on estrogen deficiency-induced osteoporosis in rats by GC/TOF-MS. Eur J Pharmacol. 2013; 718(1-3):524-32. DOI: 10.1016/j.ejphar.2013.06.030. View

15.

Li Y, Jin W, Cheng Y, Zhu W . Effect of the Associated Methanogen Methanobrevibacter thaueri on the Dynamic Profile of End and Intermediate Metabolites of Anaerobic Fungus Piromyces sp. F1. Curr Microbiol. 2016; 73(3):434-441. DOI: 10.1007/s00284-016-1078-9. View

16.

Ma B, Liu J, Zhang Q, Ying H, A J, Sun J . Metabolomic profiles delineate signature metabolic shifts during estrogen deficiency-induced bone loss in rat by GC-TOF/MS. PLoS One. 2013; 8(2):e54965. PMC: 3567117. DOI: 10.1371/journal.pone.0054965. View

17.

Thevenot E, Roux A, Xu Y, Ezan E, Junot C . Analysis of the Human Adult Urinary Metabolome Variations with Age, Body Mass Index, and Gender by Implementing a Comprehensive Workflow for Univariate and OPLS Statistical Analyses. J Proteome Res. 2015; 14(8):3322-35. DOI: 10.1021/acs.jproteome.5b00354. View

18.

Li Y, Jin W, Mu C, Cheng Y, Zhu W . Indigenously associated methanogens intensified the metabolism in hydrogenosomes of anaerobic fungi with xylose as substrate. J Basic Microbiol. 2017; 57(11):933-940. DOI: 10.1002/jobm.201700132. View

19.

Li Y, Li Y, Jin W, Sharpton T, Mackie R, Cann I . Combined Genomic, Transcriptomic, Proteomic, and Physiological Characterization of the Growth of sp. F1 in Monoculture and Co-culture With a Syntrophic Methanogen. Front Microbiol. 2019; 10:435. PMC: 6414434. DOI: 10.3389/fmicb.2019.00435. View

20.

Joblin K, Naylor G, Williams A . Effect of Methanobrevibacter smithii on Xylanolytic Activity of Anaerobic Ruminal Fungi. Appl Environ Microbiol. 1990; 56(8):2287-2295. PMC: 184724. DOI: 10.1128/aem.56.8.2287-2295.1990. View