in

The rumen microbiome inhibits methane formation through dietary choline supplementation

  • 1.

    Cubasch, U. et al. Climate Change 2013: the physical science basis. In Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Vol 1 (eds Stocker, T. F. et al.) 119–158 (Cambridge University Press, 2013).

    Google Scholar 

  • 2.

    Jackson, R. B. et al. Increasing anthropogenic methane emissions arise equally from agricultural and fossil fuel sources. Environ. Res. Lett. https://doi.org/10.1088/1748-9326/ab9ed2 (2020).

    Article 

    Google Scholar 

  • 3.

    Saunois, M. et al. The global methane budget 2000–2017. Earth Syst. Sci. Data 12, 1561–1623. https://doi.org/10.5194/essd-12-1561-2020 (2020).

    ADS 
    Article 

    Google Scholar 

  • 4.

    Hobson, P. N. & Stewart, C. S. The rumen Microbial Ecosystem (Blackie Academic & Professional, 1997).

    Book 

    Google Scholar 

  • 5.

    Henderson, G. et al. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci. Rep. 5, 14567. https://doi.org/10.1038/srep14567 (2015).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 6.

    Li, Y. et al. The complete genome sequence of the methanogenic archaeon ISO4-H5 provides insights into the methylotrophic lifestyle of a ruminal representative of the Methanomassiliicoccales. Stand. Genom. Sci. 11, 59. https://doi.org/10.1186/s40793-016-0183-5 (2016).

    Article 

    Google Scholar 

  • 7.

    Lang, K. et al. New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of “Candidatus Methanoplasma termitum”. Appl. Environ. Microbiol. 81, 1338–1352. https://doi.org/10.1128/AEM.03389-14 (2015).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 8.

    Hoehler, T., Losey, N. A., Gunsalus, R. P. & McInerney, M. J. In Biogenesis of Hydrocarbons (eds Stams, A. & Sousa, D.) 1–26 (Springer, 2018).

    Google Scholar 

  • 9.

    Neill, A. R., Grime, D. W. & Dawson, R. M. C. Conversion of choline methyl groups through trimethylamine into methane in the rumen. Biochem. J. 170, 529–535. https://doi.org/10.1042/bj1700529 (1978).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Erdman, R. A. & Sharma, B. K. Effect of dietary rumen-protected choline in lactating dairy cows. J. Dairy Sci. 74, 1641–1647. https://doi.org/10.3168/jds.S0022-0302(91)78326-4 (1991).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 11.

    Sharma, B. K. & Erdman, R. A. Effects of dietary and abomasally infused choline on milk production responses of lactating dairy cows. J. Nutr. 119, 248–254. https://doi.org/10.1093/jn/119.2.248 (1989).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 12.

    Soliva, C. & Hess, H. In Measuring Methane Production from Ruminants: Measuring Methane Emission of Ruminants by In Vitro and In Vivo Techniques (eds Makkar, H. P. & Vercoe, P. E.) 15–31 (Springer, 2007).

    Chapter 

    Google Scholar 

  • 13.

    Craciun, S. & Balskus, E. P. Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme. PNAS 109, 21307–21312. https://doi.org/10.1073/pnas.1215689109 (2012).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Jameson, E. et al. Anaerobic choline metabolism in microcompartments promotes growth and swarming of Proteus mirabilis. Environ. Microbiol. 18, 2886–2898. https://doi.org/10.1111/1462-2920.13059 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 15.

    Herring, T. I., Harris, T. N., Chowdhury, C., Mohanty, S. K. & Bobik, T. A. A bacterial microcompartment is used for choline fermentation by Escherichia coli 536. J. Bacteriol. 200, e00764-e817. https://doi.org/10.1128/JB.00764-17 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 16.

    EFSA. Scientific Opinion on safety and efficacy of choline chloride as a feed additive for all animal species. EFSA J. 9, 2353 (2011).

    Google Scholar 

  • 17.

    Lewis, D. J. Ammonia toxicity in the ruminant. J. Agric. Sci. 55, 111–117 (1960).

    CAS 
    Article 

    Google Scholar 

  • 18.

    Hogan, J. P. Absorption of ammonia through rumen of sheep. Aust. J. Biol. Sci. 14, 448–450. https://doi.org/10.1071/Bi9610448 (1961).

    CAS 
    Article 

    Google Scholar 

  • 19.

    Sprott, G. D. & Patel, G. B. Ammonia toxicity in pure cultures of methanogenic bacteria. Syst. Appl. Microbiol. 7, 358–363 (1986).

    CAS 
    Article 

    Google Scholar 

  • 20.

    Lewis, D. Ammonia toxicity in the ruminant. J. Agric. Sci. 55(1), 111–117 (1960).

    CAS 
    Article 

    Google Scholar 

  • 21.

    Ungerfeld, E. M., Rust, S. R. & Burnett, R. Increases in microbial nitrogen production and efficiency in vitro with three inhibitors of ruminal methanogenesis. Can. J. Microbiol. 53, 496–503. https://doi.org/10.1139/W07-008 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 22.

    Lundgren, B. R., Sarwar, Z., Pinto, A., Ganley, J. G. & Nomura, C. T. Ethanolamine catabolism in Pseudomonas aeruginosa PAO1 is regulated by the enhancer-binding protein EatR (PA4021) and the alternative sigma factor RpoN. J. Bacteriol. 198, 2318–2329. https://doi.org/10.1128/JB.00357-16 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 23.

    Rychlik, J. L., LaVera, R. & Russell, J. B. Amino acid deamination by ruminal Megasphaera elsdenii strains. Curr. Microbiol. 45, 340–345. https://doi.org/10.1007/s00284-002-3743-4 (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 24.

    Park, K. & Lee, H. Effects of nitrogen gas flushing in comparison with argon on rumen fermentation characteristics in in vitro studies. J. Anim. Sci. Technol. 62, 52–57. https://doi.org/10.5187/jast.2020.62.1.52 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25.

    Hobson, P. N., Summers, R., Postgate, J. R. & Ware, D. A. Nitrogen fixation in the rumen of a living sheep. J. Gen. Microbiol. 77, 225–226. https://doi.org/10.1099/00221287-77-1-225 (1973).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 26.

    Harada, N., Nishiyama, M. & Matsumoto, S. Inhibition of methanogens increases photo-dependent nitrogenase activities in anoxic paddy soil amended with rice straw. FEMS Microbiol. Ecol. 35, 231–238. https://doi.org/10.1111/j.1574-6941.2001.tb00808.x (2001).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 27.

    Haaker, H. & Klugkist, J. The bioenergetics of electron transport to nitrogenase. J FEMS Microbiol. Lett. 46, 57–71 (1987).

    CAS 
    Article 

    Google Scholar 

  • 28.

    Edgren, T. & Nordlund, S. The fixABCX genes in Rhodospirillum rubrum encode a putative membrane complex participating in electron transfer to nitrogenase. J. Bacteriol. 186, 2052–2060 (2004).

    CAS 
    Article 

    Google Scholar 

  • 29.

    Igai, K. et al. Nitrogen fixation and nifH diversity in human gut microbiota. Sci. Rep. 6, 31942. https://doi.org/10.1038/srep31942 (2016).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Ungerfeld, E. M. Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: A meta-analysis. Front. Microbiol. 6, 37. https://doi.org/10.3389/fmicb.2015.00037 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Leahy, S. C. et al. The complete genome sequence of Methanobrevibacter sp. AbM4. Stand. Genom. Sci. 8, 215–227. https://doi.org/10.4056/sigs.3977691 (2013).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Hoedt, E. C. et al. Differences down-under: Alcohol-fueled methanogenesis by archaea present in Australian macropodids. ISME J. 10, 2376–2388. https://doi.org/10.1038/ismej.2016.41 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 33.

    Ungerfeld, E. M. & Kohn, R. A. In Ruminant Physiology: Digestion, Metabolism and Impact of Nutrition on Gene Expression, Immunology and Stress (eds Sejrsen, K. et al.) 55–85 (Wageningen Academic Publishers, 2006).

    Google Scholar 

  • 34.

    van Zijderveld, S. M. et al. Nitrate and sulfate: Effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. J. Dairy Sci. 93, 5856–5866. https://doi.org/10.3168/jds.2010-3281 (2010).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 35.

    Lan, W. & Yang, C. Ruminal methane production: Associated microorganisms and the potential of applying hydrogen-utilizing bacteria for mitigation. Sci. Total Environ. 654, 1270–1283. https://doi.org/10.1016/j.scitotenv.2018.11.180 (2019).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 36.

    Loubinoux, J., Bronowicki, J. P., Pereira, I. A., Mougenel, J. L. & Faou, A. E. Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases. FEMS Microbiol. Ecol. 40, 107–112. https://doi.org/10.1111/j.1574-6941.2002.tb00942.x (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 37.

    Gould, D. H., Cummings, B. A. & Hamar, D. W. In vivo indicators of pathologic ruminal sulphide production in steers with diet-induced polioencephalomalacia. J. Vet. Diagn. Invest. 9, 72–76. https://doi.org/10.1177/104063879700900113 (1997).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 38.

    Anderson, R. C., Rasmussen, M. A., Jensen, N. S. & Allison, M. J. Denitrobacterium detoxificans gen. nov., sp. nov., a ruminal bacterium that respires on nitrocompounds. Int. J. Syst. Evol. Microbiol. 50(Pt 2), 633–638. https://doi.org/10.1099/00207713-50-2-633 (2000).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 39.

    Anderson, R. C. et al. Ruminal fermentation of anti-methanogenic nitrate- and nitro-containing forages in vitro. Front. Vet. Sci. 3, 62. https://doi.org/10.3389/fvets.2016.00062 (2016).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    Zhang, Z. W. et al. Nitrocompounds as potential methanogenic inhibitors in ruminant animals: A review. Anim. Feed Sci. Tech. 236, 107–114. https://doi.org/10.1016/j.anifeedsci.2017.12.010 (2018).

    CAS 
    Article 

    Google Scholar 

  • 41.

    Marounek, M., Fliegrova, K. & Bartos, S. Metabolism and some characteristics of ruminal strains of Megasphaera elsdenii. Appl. Environ. Microbiol. 55, 1570–1573. https://doi.org/10.1128/AEM.55.6.1570-1573.1989 (1989).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Hackmann, T. J., Ngugi, D. K., Firkins, J. L. & Tao, J. Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids. Environ. Microbiol. 19, 4670–4683. https://doi.org/10.1111/1462-2920.13929 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Janssen, P. H. Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Anim. Feed Sci. Technol. 160, 1–22. https://doi.org/10.1016/j.anifeedsci.2010.07.002 (2010).

    CAS 
    Article 

    Google Scholar 

  • 44.

    Greening, C. et al. Diverse hydrogen production and consumption pathways influence methane production in ruminants. ISME J. 13, 2617–2632. https://doi.org/10.1038/s41396-019-0464-2 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Gilmour, M., Flint, H. J. & Mitchell, W. J. Multiple lactate dehydrogenase activities of the rumen bacterium Selenomonas ruminantium. Microbiol. 140(Pt 8), 2077–2084. https://doi.org/10.1099/13500872-140-8-2077 (1994).

    CAS 
    Article 

    Google Scholar 

  • 46.

    Chowdhury, N. P., Kahnt, J. & Buckel, W. Reduction of ferredoxin or oxygen by flavin-based electron bifurcation in Megasphaera elsdenii. FEBS J. 282, 3149–3160. https://doi.org/10.1111/febs.13308 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 47.

    Weghoff, M. C., Bertsch, J. & Muller, V. A novel mode of lactate metabolism in strictly anaerobic bacteria. Environ. Microbiol. 17, 670–677. https://doi.org/10.1111/1462-2920.12493 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 48.

    Hernandez, J., Benedito, J. L., Abuelo, A. & Castillo, C. Ruminal acidosis in feedlot: from aetiology to prevention. Sci. World J. 2014, 702572. https://doi.org/10.1155/2014/702572 (2014).

    Article 

    Google Scholar 

  • 49.

    Vuotto, C., Barbanti, F., Mastrantonio, P. & Donelli, G. Lactobacillus brevis CD2 inhibits Prevotella melaninogenica biofilm. Oral Dis. 20, 668–674. https://doi.org/10.1111/odi.12186 (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 50.

    van Lingen, H. J. et al. Thermodynamic driving force of hydrogen on rumen microbial metabolism: A theoretical investigation. PLoS One 11, e0161362. https://doi.org/10.1371/journal.pone.0161362 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 51.

    Ungerfeld, E. M., Aedo, M. F., Martinez, E. D. & Saldivia, M. Inhibiting methanogenesis in rumen batch cultures did not increase the recovery of metabolic hydrogen in microbial amino acids. Microorganisms 7, 155. https://doi.org/10.3390/microorganisms7050115 (2019).

    CAS 
    Article 

    Google Scholar 

  • 52.

    Ng, F. et al. An adhesin from hydrogen-utilizing rumen methanogen Methanobrevibacter ruminantium M1 binds a broad range of hydrogen-producing microorganisms. Environ. Microbiol. 18, 3010–3021. https://doi.org/10.1111/1462-2920.13155 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 53.

    Soliva, C. R., Amelchanka, S. L., Duval, S. M. & Kreuzer, M. Ruminal methane inhibition potential of various pure compounds in comparison with garlic oil as determined with a rumen simulation technique (Rusitec). Brit. J. Nutr. 106, 114–122. https://doi.org/10.1017/S0007114510005684 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 54.

    Terranova, M. et al. Increasing the proportion of hazel leaves in the diet of dairy cows reduced methane yield and excretion of nitrogen in volatile form, but not milk yield. Anim. Feed Sci. Technol. 276, 114796. https://doi.org/10.1016/j.anifeedsci.2020.114790 (2021).

    CAS 
    Article 

    Google Scholar 

  • 55.

    Ehrlich, G. G., Goerlitz, D. F., Bourell, J. H., Eisen, G. V. & Godsy, E. M. Liquid chromatographic procedure for fermentation product analysis in the identification of anaerobic bacteria. Appl. Environ. Microbiol. 42, 878–885 (1981).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 56.

    Bica, R. et al. Nuclear magnetic resonance to detect rumen metabolites associated with enteric methane emissions from beef cattle. Sci. Rep. 10, 5578. https://doi.org/10.1038/s41598-020-62485-y (2020).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 57.

    Henderson, G. et al. Effect of DNA extraction methods and sampling techniques on the apparent structure of cow and sheep rumen microbial communities. PLoS One 8, e74787. https://doi.org/10.1371/journal.pone.0074787 (2013).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 58.

    Kittelmann, S. et al. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS One 8, e47879. https://doi.org/10.1371/journal.pone.0047879 (2013).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 59.

    Milanese, A. et al. Microbial abundance, activity and population genomic profiling with mOTUs2. Nat. Comm. 10, 1014. https://doi.org/10.1038/s41467-019-08844-4 (2019).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 60.

    Paoli, L. et al. Uncharted biosynthetic potential of the ocean microbiome. bioRxiv https://doi.org/10.1101/2021.03.24.436479 (2021).

    Article 

    Google Scholar 

  • 61.

    Bushnell, B. BBMap: A fast, accurate, splice-aware aligner. in 9th Annual Genomics of Energy & Environment Meeting. (Lawrence Berkeley National Lab (LBNL), Berkeley, CA, USA). https://www.osti.gov/servlets/purl/1241166 (2014).

  • 62.

    Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: A new versatile metagenomic assembler. Genome Res. 27, 824–834. https://doi.org/10.1101/gr.213959.116 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 63.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760. https://doi.org/10.1093/bioinformatics/btp324 (2009).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Kang, D. D. et al. MetaBAT 2: An adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7, e7359. https://doi.org/10.7717/peerj.7359 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 65.

    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055. https://doi.org/10.1101/gr.186072.114 (2015).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 66.

    Seshadri, R. et al. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nat. Biotechnol. 36, 359–367. https://doi.org/10.1038/nbt.4110 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Stewart, R. D. et al. Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery. Nat. Biotechnol. 37, 953–961. https://doi.org/10.1038/s41587-019-0202-3 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 68.

    Hyatt, D. et al. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 11, 119. https://doi.org/10.1186/1471-2105-11-119 (2010).

    CAS 
    Article 

    Google Scholar 

  • 69.

    Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152. https://doi.org/10.1093/bioinformatics/bts565 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 70.

    Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acid Res. 28, 27–30. https://doi.org/10.1093/nar/28.1.27 (2000).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 71.

    Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60. https://doi.org/10.1038/nmeth.3176 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 72.

    Li, L., Stoeckert, C. J. Jr. & Roos, D. S. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189. https://doi.org/10.1101/gr.1224503 (2003).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 73.

    Allen, B., Drake, M., Harris, N. & Sullivan, T. Using KBase to assemble and annotate prokaryotic genomes. Curr. Protoc. Microbiol. 46, 1E 13 11-11E 13 18. https://doi.org/10.1002/cpmc.37 (2017).

    Article 

    Google Scholar 

  • 74.

    RStudio Team. R Studio: Integrated development environment for R. Version 1.4.1106 (2021).

  • 75.

    Oksanen, J. et al. The vegan package. Community Ecol. Pack. 10, 631–637 (2007).

    Google Scholar 

  • 76.

    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. https://doi.org/10.1186/s13059-014-0550-8 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    Functional diversity effects on productivity increase with age in a forest biodiversity experiment

    MIT Energy Night 2021: Connecting global innovators to local talent