Addressing global ruminant agricultural challenges through understanding the rumen microbiome: Past, present, and future Sharon A. Huws, Christopher J. Creevey, Linda B. Oyama, Itzhak Mizrahi, Stuart E. Denman, Milka Popova, Rafael Munoz Tamayo, Evelyne Forano, Sinead M. Waters, Matthias Hess, et al. To cite this version: Sharon A. Huws, Christopher J. Creevey, Linda B. Oyama, Itzhak Mizrahi, Stuart E. Den- man, et al.. Addressing global ruminant agricultural challenges through understanding the ru- men microbiome: Past, present, and future. Frontiers in Microbiology, Frontiers Media, 2018, 9, 10.3389/fmicb.2018.02161. hal-01890696 HAL Id: hal-01890696 https://hal.archives-ouvertes.fr/hal-01890696 Submitted on 8 Oct 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License REVIEW published: 25 September 2018 doi: 10.3389/fmicb.2018.02161 Addressing Global Ruminant Agricultural Challenges Through Understanding the Rumen Microbiome: Past, Present, and Edited by: Future Zhongtang Yu, The Ohio State University, Sharon A. Huws 1*, Christopher J. Creevey 1, Linda B. Oyama 1, Itzhak Mizrahi 2, United States Stuart E. Denman 3, Milka Popova 4, Rafael Muñoz-Tamayo 5, Evelyne Forano 6, Reviewed by: Sinead M. Waters 7, Matthias Hess 8, Ilma Tapio 9, Hauke Smidt 10, Sophie J. Krizsan 11, Shengguo Zhao, David R. Yáñez-Ruiz 12, Alejandro Belanche 12, Leluo Guan 13, Robert J. Gruninger 14, Institute of Animal Sciences, Chinese Tim A. McAllister 14, C. Jamie Newbold 15, Rainer Roehe 15, Richard J. Dewhurst 15, Academy of Agricultural Sciences, 16 17 18 19 China Tim J. Snelling , Mick Watson , Garret Suen , Elizabeth H. Hart , 19 1 20 20 Suzanne Lynn Ishaq, Alison H. Kingston-Smith , Nigel D. Scollan , Rodolpho M. do Prado , Eduardo J. Pilau , 21 22 23 24 University of Oregon, United States Hilario C. Mantovani , Graeme T. Attwood , Joan E. Edwards , Neil R. McEwan , Steven Morrisson 25, Olga L. Mayorga 26, Christopher Elliott 1 and Diego P. Morgavi 4 *Correspondence: Sharon A. Huws 1 Institute for Global Food Security, Queen’s University of Belfast, Belfast, United Kingdom, 2 Department of Life Sciences and [email protected] the National Institute for Biotechnology in the Negev, Ben Gurion University of the Negev, Beer Sheva, Israel, 3 Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Queensland Bioscience Precinct, St Specialty section: Lucia, QLD, Australia, 4 Institute National de la Recherche Agronomique, UMR1213 Herbivores, Clermont Université, VetAgro This article was submitted to Sup, UMR Herbivores, Clermont-Ferrand, France, 5 UMR Modélisation Systémique Appliquée aux Ruminants, INRA, Microbial Symbioses, AgroParisTech, Université Paris-Saclay, Paris, France, 6 UMR 454 MEDIS, INRA, Université Clermont Auvergne, a section of the journal Clermont-Ferrand, France, 7 Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Frontiers in Microbiology Centre, Grange, Ireland, 8 College of Agricultural and Environmental Sciences, University of California, Davis, Davis, CA, United States, 9 Natural Resources Institute Finland, Jokioinen, Finland, 10 Department of Agrotechnology and Food Sciences, Received: 31 May 2018 Wageningen, Netherlands, 11 Department of Agricultural Research for Northern Sweden, Swedish University of Agricultural Accepted: 23 August 2018 Sciences, Umeå, Sweden, 12 Estacion Experimental del Zaidin, Consejo Superior de Investigaciones Cientificas, Granada, Published: 25 September 2018 Spain, 13 Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada, Citation: 14 Lethbridge Research Centre, Agriculture and Agri-Food Canada, Lethbridge, AB, Canada, 15 Scotland’s Rural College, Huws SA, Creevey CJ, Oyama LB, Edinburgh, United Kingdom, 16 The Rowett Institute, University of Aberdeen, Aberdeen, United Kingdom, 17 The Roslin Mizrahi I, Denman SE, Popova M, Institute and the Royal (Dick) School of Veterinary Studies (R(D)SVS), University of Edinburgh, Edinburgh, United Kingdom, Muñoz-Tamayo R, Forano E, 18 Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, United States, 19 Institute of Biological, Waters SM, Hess M, Tapio I, Smidt H, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom, 20 Laboratório de Biomoléculas e Krizsan SJ, Yáñez-Ruiz DR, Espectrometria de Massas-Labiomass, Departamento de Química, Universidade Estadual de Maringá, Maringá, Brazil, Belanche A, Guan L, Gruninger RJ, 21 Department of Microbiology, Universidade Federal de Viçosa, Viçosa, Brazil, 22 AgResearch Limited, Grasslands Research McAllister TA, Newbold CJ, Roehe R, Centre, Palmerston North, New Zealand, 23 Laboratory of Microbiology, Wageningen University & Research, Wageningen, Dewhurst RJ, Snelling TJ, Watson M, Netherlands, 24 School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen, United Kingdom, 25 Sustainable Suen G, Hart EH, Kingston-Smith AH, Livestock, Agri-Food and Bio-Sciences Institute, Hillsborough, United Kingdom, 26 Colombian Agricultural Research Scollan ND, do Prado RM, Pilau EJ, Corporation, Mosquera, Colombia Mantovani HC, Attwood GT, Edwards JE, McEwan NR, Morrisson S, Mayorga OL, Elliott C The rumen is a complex ecosystem composed of anaerobic bacteria, protozoa, fungi, and Morgavi DP (2018) Addressing methanogenic archaea and phages. These microbes interact closely to breakdown Global Ruminant Agricultural Challenges Through Understanding plant material that cannot be digested by humans, whilst providing metabolic energy the Rumen Microbiome: Past, to the host and, in the case of archaea, producing methane. Consequently, ruminants Present, and Future. Front. Microbiol. 9:2161. produce meat and milk, which are rich in high-quality protein, vitamins and minerals, doi: 10.3389/fmicb.2018.02161 and therefore contribute to food security. As the world population is predicted to Frontiers in Microbiology | www.frontiersin.org 1 September 2018 | Volume 9 | Article 2161 Huws et al. Understanding the Rumen Microbiome reach approximately 9.7 billion by 2050, an increase in ruminant production to satisfy global protein demand is necessary, despite limited land availability, and whilst ensuring environmental impact is minimized. Although challenging, these goals can be met, but depend on our understanding of the rumen microbiome. Attempts to manipulate the rumen microbiome to benefit global agricultural challenges have been ongoing for decades with limited success, mostly due to the lack of a detailed understanding of this microbiome and our limited ability to culture most of these microbes outside the rumen. The potential to manipulate the rumen microbiome and meet global livestock challenges through animal breeding and introduction of dietary interventions during early life have recently emerged as promising new technologies. Our inability to phenotype ruminants in a high-throughput manner has also hampered progress, although the recent increase in “omic” data may allow further development of mathematical models and rumen microbial gene biomarkers as proxies. Advances in computational tools, high-throughput sequencing technologies and cultivation-independent “omics” approaches continue to revolutionize our understanding of the rumen microbiome. This will ultimately provide the knowledge framework needed to solve current and future ruminant livestock challenges. Keywords: rumen, microbiome, host, diet, production, methane, omics GLOBAL AGRICULTURAL CHALLENGES steers (with 0 being the expected and values <0 inferring that the animal has greater feed efficiency than expected), There are currently 7.5 billion humans on the planet, and resulting in high RFI animals requiring approximately 1,000 kg the world Hunger Map estimates that 795 million people more feed/annum than low RFI animals to achieve the (over 10%) do not have access to sufficient food (WFP, same production parameters (Fouhse et al., 2017). Therefore, 2015). Whilst some models predict the world population to understanding the underlying mechanisms for RFI, particularly peak at 9.7 billion in 2050, others estimate a population with respect to the involvement of the rumen microbiome, of 11.2 billion in 2100 (United Nations, 2015). To meet could aid efficiency and sustainability of ruminant production an increasing demand for food, the Food and Agriculture (Mizrahi, 2011). Organization of the United Nations (FAO) predicts that total Ruminant livestock production has been estimated to be agricultural production (including crops and animals) will responsible for approximately 14% of anthropogenic methane, need to be 60% higher than in 2005. With animal protein a potent greenhouse gas (GHG), released annually into the demand rising at a proportionally faster rate, estimates suggest atmosphere due to the activity of rumen methanogens (Gerber that global meat and milk production will have to increase et al., 2013). The released methane, produced by