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Fmicb-10-02207.Pdf UCC Library and UCC researchers have made this item openly available. Please let us know how this has helped you. Thanks! Title Use of lactic acid bacteria to reduce methane production in ruminants, a critical review Author(s) Doyle, Natasha; Mbandlwa, Philiswa; Kelly, William J.; Attwood, Graeme; Li, Yang; Ross, R. Paul; Stanton, Catherine; Leahy, Sinead Publication date 2019-09-09 Original citation Doyle, N., Mbandlwa, P., Kelly, W. J., Attwood, G., Li, Y., Ross, R. P., Stanton, C. and Leahy, S. (2019) 'Use of Lactic Acid Bacteria to Reduce Methane Production in Ruminants, a Critical Review', Frontiers in Microbiology, 10, 2207 (13pp.) DOI: 10.3389/fmicb.2019.02207 Type of publication Article (peer-reviewed) Link to publisher's https://www.frontiersin.org/articles/10.3389/fmicb.2019.02207/full version http://dx.doi.org/10.3389/fmicb.2019.02207 Access to the full text of the published version may require a subscription. Rights ©2019 Doyle, Mbandlwa, Kelly, Attwood, Li, Ross, Stanton and Leahy. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. http://creativecommons.org/licenses/by/4.0/ Item downloaded http://hdl.handle.net/10468/8748 from Downloaded on 2021-09-30T19:28:23Z fmicb-10-02207 October 1, 2019 Time: 13:9 # 1 MINI REVIEW published: 01 October 2019 doi: 10.3389/fmicb.2019.02207 Use of Lactic Acid Bacteria to Reduce Methane Production in Ruminants, a Critical Review Natasha Doyle1,2†, Philiswa Mbandlwa2†, William J. Kelly3†, Graeme Attwood4, Yang Li4, R. Paul Ross2,5, Catherine Stanton1,5 and Sinead Leahy4* 1 Teagasc Moorepark Food Research Centre, Fermoy, Ireland, 2 School of Microbiology, University College Cork, Cork, Ireland, 3 Donvis Ltd., Palmerston North, New Zealand, 4 AgResearch Limited, Grasslands Research Centre, Palmerston North, New Zealand, 5 APC Microbiome Ireland, University College Cork, Cork, Ireland Enteric fermentation in ruminants is the single largest anthropogenic source of agricultural methane and has a significant role in global warming. Consequently, innovative solutions to reduce methane emissions from livestock farming are required to ensure future sustainable food production. One possible approach is the use of lactic Edited by: acid bacteria (LAB), Gram positive bacteria that produce lactic acid as a major end David R. Yanez-Ruiz, product of carbohydrate fermentation. LAB are natural inhabitants of the intestinal tract Estación Experimental del Zaidín (CSIC), Spain of mammals and are among the most important groups of microorganisms used in Reviewed by: food fermentations. LAB can be readily isolated from ruminant animals and are currently Elvira Maria Hebert, used on-farm as direct-fed microbials (DFMs) and as silage inoculants. While it has been National Scientific and Technical Research Council (CONICET), proposed that LAB can be used to reduce methane production in ruminant livestock, Argentina so far research has been limited, and convincing animal data to support the concept Timothy John Snelling, are lacking. This review has critically evaluated the current literature and provided a Harper Adams University, United Kingdom comprehensive analysis and summary of the potential use and mechanisms of LAB as *Correspondence: a methane mitigation strategy. It is clear that although there are some promising results, Sinead Leahy more research is needed to identify whether the use of LAB can be an effective methane [email protected] mitigation option for ruminant livestock. †These authors have contributed equally to this work Keywords: lactic acid bacteria, methane, methanogens, bacteriocins, direct-fed microbials, silage inoculants, mitigation Specialty section: This article was submitted to Systems Microbiology, INTRODUCTION a section of the journal Frontiers in Microbiology While ruminant animals play an important role in sustainable agricultural systems (Eisler et al., Received: 12 April 2019 2014) they are also an important source of greenhouse gas (GHG) emissions (Reisinger and Clark, Accepted: 09 September 2019 2018). Regardless of the ruminant species, the largest source of GHG emissions from ruminant Published: 01 October 2019 production is methane (CH4), with more than 90 percent of emissions originating from enteric Citation: fermentation (Opio et al., 2013). Enteric fermentation is a digestive process by which a community Doyle N, Mbandlwa P, Kelly WJ, of microbes present in the forestomach of ruminants (the reticulo-rumen) break down plant Attwood G, Li Y, Ross RP, Stanton C material into nutrients that can be used by the animal for the production of high-value proteins and Leahy S (2019) Use of Lactic Acid Bacteria to Reduce Methane that include milk, meat and leather products. Hydrogen (H2) and methyl-containing compounds Production in Ruminants, a Critical generated as fermentation end products of this process are used by different groups of rumen Review. Front. Microbiol. 10:2207. methanogenic archaea to form CH4, which is belched and exhaled from the lungs via respiration doi: 10.3389/fmicb.2019.02207 from the animal and released to the atmosphere. In the coming decades, livestock farmers will face Frontiers in Microbiology| www.frontiersin.org 1 October 2019| Volume 10| Article 2207 fmicb-10-02207 October 1, 2019 Time: 13:9 # 2 Doyle et al. Lactic Acid Bacteria and Methane numerous challenges and the development of technologies and LAB and the Rumen practices which support efficient sustainable food production LAB are members of the normal gastrointestinal tract microbiota, while moderating greenhouse gas emissions are urgently however, in ruminants these organisms are generally only required. More than 100 countries have committed to reducing prevalent in young animals before the rumen has properly agricultural GHG emissions in the 2015 Paris Agreement of developed (Stewart et al., 1988). LAB are unable to initiate the United Nations Framework Convention on Climate Change, the metabolism of plant structural polysaccharides and are however, known agricultural practices could deliver just 21– not regarded as major contributors to rumen fermentation. In 40% of the needed reduction, even if implemented fully the Global Rumen Census project (Henderson et al., 2015) at scale (Wollenberg et al., 2016). New technical mitigation which profiled the microbial community of 684 rumen samples options are needed. Reviews of CH4 mitigation strategies collected from a range of ruminant species, only members of the consistently discuss the possibility that lactic acid bacteria genus Streptococcus were found in a majority of samples (63% (LAB) could be used to modulate rumen microbial communities prevalence, 0.5% abundance). Nevertheless, LAB can be readily thus providing a practical and effective on-farm approach to isolated from the rumen, with some species such as Lactobacillus reducing CH4 emissions from ruminant livestock (Hristov et al., ruminis and Streptococcus equinus (formerly S. bovis) being 2013; Takahashi, 2013; Knapp et al., 2014; Jeyanathan et al., regarded as true rumen inhabitants while others (Lactobacillus 2014; Varnava et al., 2017). This review examines the possible plantarum and Lactococcus lactis) are likely to be transient contribution of LAB in the development of an on-farm CH4 bacteria that have been introduced with the feed (Stewart, 1992). mitigating strategy. Several obligately anaerobic rumen bacteria also produce lactate as a fermentation end product and two of these are included RESULTS AND DISCUSSION in this review. These organisms (Kandleria vitulina and Sharpea azabuensis) are both members of the family Erysipelotrichaceae General Characteristics of Lactic Acid within the phylum Firmicutes, although Kandleria vitulina was formerly known as Lactobacillus vitulinus (Salvetti et al., Bacteria 2011). Sharpea and Kandleria are a significant component of Lactic acid bacteria are Gram positive, acid tolerant, facultatively the rumen microbiome in low CH4 yield animals in which anaerobic bacteria that produce lactic acid as a major end- rapid heterofermentative growth results in lactate production product of carbohydrate fermentation (Stilez and Holzapfel, (Kamke et al., 2016). 1997). Biochemically they include homofermenters that produce Table 1 lists the rumen LAB together with strains of Kandleria primarily lactic acid, and heterofermenters that also give a and Sharpea that have been genome sequenced along with variety of other fermentation end-products such as acetic acid, potential antimicrobial biosynthetic clusters predicted from the ethanol and CO2. LAB have long been used as starter cultures genome sequence data. The majority (81%) of genome sequenced for a wide range of dairy, meat and plant fermentations, and strains from rumen members of the Streptococcaceae encode this history of use in human and animal foods has resulted antimicrobial biosynthetic clusters, and previous studies have in most LAB having Qualified Presumption of Safety (QPS) also reported that rumen streptococci can produce a range of status in the European Union or Generally Recognized as Safe bacteriocins (Iverson and Mills, 1976; Mantovani et al., 2001; (GRAS) status in the United
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