Microbial hydrogen utilisation

It is generally accepted that an increase in the partial pressure of [H] within the rumen will result in an inhibition of fermentation through reduced re-oxidisation of co-factors (Ungerfeld, 2015b). Additionally, stoichiometry shows that a decrease in enteric CH4 production from ruminants should result in more energy for maintenance and production (Johnson and Johnson, 1995). However, these two concepts are not always observed as responses to a reduction in enteric CH4 production.

Hydrogenotrophic archaea (Methanobrevibacter, Methanobacterium) are the predominant archaea (Henderson et al., 2015) and can utilise [H] or to a much lesser extent formate, as sources of electrons to reduce C02 to CH4 (Richards etal., 2016). The contribution of formate to CH4 production is estimated at 18% of CH4 produced in the rumen (Tapio et al., 2017b). Methylotrophic methanogens (i.e. Methanosarcinales, Methanosphaera and Methanomassiliicoccaceae) are less abundant and can utilise methanol and methylamines to produce CH4 (Huws et al., 2018). The acetoclastic pathway can also result in the formation of CH4 from acetate, but the Methanosarcinales spp. which utilise this pathway have a slow growth rate and are not prominent within the mature rumen (Friedman et al„ 2017b). Whilst the majority of [H] is utilised by archaea, several other means of [H] disposal may occur in the rumen, including the use of reducing equivalents to reduce sulphate and nitrate (N03~) as well as reductive acetogenesis, propionogenesis and the synthesis of microbial biomass.

Sulphate and N03~ reduction reactions are more thermodynamically favourable than the reduction of C02 (Morgavi et al., 2010; Haque, 2018) and sulphate and N03' reducing bacteria have been shown to outcompete methanogens in anoxic environments (Scheid et al., 2003). Reductive acetogenesis is not as thermodynamically favourable as methanogenesis and it is unlikely that the rumen would establish a dominant and sustained microbial population capable of this process (Fonty et al., 2007; Friedman et al., 2017b). However, if a reductive acetogen was developed that could exist naturally in the rumen and utilise only [H], rather than sugars (obligate hydrogenotroph), it could potentially act as a successful [H] sink and suppress methanogenesis (Ungerfeld, 2015a).

Feed additives which redirect [H] towards an alternative metabolic sink represent a new avenue for investigation. Martinez-Fernandez et al. (2017) supplemented Brahman steers with the antimethanogenic compound, chloroform. Half of the steers were also administered phloroglucinol, an intermediate metabolite of flavonoid degradation which through the utilisation [H] and formate can form acetate. Phloroglucinol resulted in an increase in acetate production, Prevotella, Ruminococcus and Fibrobacter abundance as well as a decrease in H2 and formate production. This study was the first in vivo trial to demonstrate that [H] can be redirected towards the reduction phloroglucinol as a means of inhibiting methanogenesis. Further studies examining the redirection of [H] during the inhibition of methanogenesis, and how this alters the rumen microbiome are needed. For example, 3-NOP can successfully decrease methanogenesis; however, excess [H] is not captured through other reductive process and the H2 emission is increased. Redirection of this [H] into a usable metabolite would result in a further reduction of CH4 production and CH4 intensity, potentially without the loss of energy in the form of H2.

It has been suggested that, as within other anaerobic environments, there is a balance between methane producing and methane utilising microbes. Methanotrophs are specific archaea or bacteria which can metabolise CH4 in the presence of oxygen (Leng, 2014). However, CH4 can also be anaerobically oxidised utilising existing oxygen within sulphate, metal oxides and nitrate (Joye, 2012). Their presence or importance in the ruminal environment is a matter of debate.

In an artificial rumen system, it was found that only 0.2-0.5% of CH4 produced was oxidised by coupling with sulphate reduction (Kajikawa et al., 2003). However, it is theorised that methanotrophs are more likely to colonise the rumen wall due to diffusion of oxygen from the bloodstream. A metagenomic analysis of the microbial populations in beef cattle rumen did not detect methanotrophs (Wallace et al., 2015). Using methanotroph-specific primers, Mitsumori et al. (2002) suggested that methanotrophs exist in both ruminal fluid and the biofilm attached to the rumen wall, but only type I methanotrophs were detected. Type I methanotrophs include Methylomonas, Methylobacter, Methylomicrobium and Methylococcus which utilise the ribulose monophosphate pathway to assimilate carbon. Type II includes Methylocystis and Methylosinus, which use the serine pathway to assimilate carbon (Mitsumori et al., 2002). Jin et al.

(2017) found that the Methylococcaceae family was dominant in solid, liquid and rumen wall-associated populations. In rumen batch culture, Liu etal.(2017) found that the addition of N03~ decreased methanogenesis and increased the phylum NC10.The NC10 bacteria are the only known bacteria that are capable of anaerobic oxidisation of CH4. The bacterium Methoxymirabilis oxyfera converts N02' to nitric oxide and then dismutates nitric oxide into nitrogen and oxygen, using the resulting 02 to support CH4 oxidation (He et al., 2016; Joye, 2012). All other microbes with the ability to anaerobically oxidise CH4 are archaea. Klieve et al. (2012) identified that rumen contents of cattle had mcrA gene sequences relating to CH4 oxidising archaea, represented by archaea which have been shown to anaerobically catabolise methane using sulphate reduction in sediments from the Gulf of Mexico (Lloyd et al., 2006).

Parmar et al. (2015) established that Type I methanotrophs were more abundant in 50:50 forage-to-concentrate diets, whereas Type II increased in a complete forage diet. The enzyme formate dehydrogenase, which oxidises formate, was increased within the high-forage diet, a finding consistent with an increase in Type II methanotrophs. Auffret et al. (2018) also identified the presence of three methanotrophic bacteria including Methylobacterium, Methylomonas and Methylomicrobium in low abundance (0.1 ±0.01%) in the rumen of beef steers. The Methylomonas were more abundant and negatively correlated with CH4 emissions. The overall diversity of methanotrophs was greater in high CH4 emitters as compared to low emitters. The inconsistency in the identification of methanotrophs in the rumen could reflect the lack of sequencing depth and breadth for these rare populations.

The importance of methanotrophs in a nutrient-rich environment like the rumen is questionable. However, the use of CH4 by methanotrophs may partially account for [H] that is not stoichiometrically accounted for when CH4 inhibitors such as N03' and 3-NOP are included in ruminant diets. Methanotrophs are important in other anaerobic environments such as sediments, the oceanic seafloor and both freshwater and saline water systems (He et al.,2016), oxidising over 80% of the emitted CH4 before it reaches the atmosphere (Cai et al., 2016). However, these are relatively stable environments, and do not experience the same passage rate or daily variation in substrate availability as within the rumen. As sequencing technologies improve our ability to delve deeper into the ruminal microbiome, a more detailed identification of methanotrophs should enhance our understanding of [H] balance in the rumen.

Future trends and conclusion

Presently, 3-NOP and N03“ can mitigate enteric CH4 production while having little effects on GHG emissions from manure; however, the excess [H] is not completely captured in the form of reduced substrates (Table 1). Likewise,

Nutritional factors affecting greenhouse gas production from ruminants

Table 1 Summary of dietary additives and their implications for GHG mitigation from ruminant production

Dietary

additive

Enteric

emissions

Improvement in product

Manure

emissions

Improvement in product

Interaction

Recommend

Nitro compounds

Nitrate

ICH,

TH.

No

N/A may

tn2o, |nh3

N/A

N/A, Likely Yes[1]

3 - NOP

ICH,

TH.

Inconsistent

N/A

N/A

N/A,

Unlikely

Yes[1]

Secondary compounds

Tannins

Variable, may |CH4

Inconsistent, may J.DMI

TNO.

TNH3"

Yes

Yes

Too variable

Organic carbon

Humic

substances

No

N/A

N/Ae, may |NH3

N/A[1], may T stable C

No

N/A

Biochar

No

N/A

N/A[1] may |N02, |NH3

N/A[1], may T stable C

N/A

N/A

e Based on limited research. N/A = information not available.

531

tannins can reduce GHG emissions from manure, whereas their effect on enteric CH4 emissions from ruminants is highly variable. Organic C additives may have potential for mitigation of manure GHG, but there is limited research to support their ability to reduce enteric CH4 emissions.

Dietary manipulation as a mitigation strategy isthoughtto be the most viable method for reducing GHG emissions from ruminants. However, as highlighted, there is a balance to be met towards ensuring disrupting rumen metabolism does not cause unintended increases in GHG from manure. There are also additional considerations for how dietary changes alter the rumen microbiome and how long these changes are sustained. Investigations regarding the effects of dietary additives on both enteric and manure CH4 emissions have reinforced the complexity of the dynamics between enteric- and manure-CH4. Though enteric CH4 production has a much larger C02-equivalent contribution to total GHG emissions, NzO produced by manure is a more potent GHG. Therefore, when recommending GHG mitigation strategies from ruminants, it is important to validate its efficiency at a whole-farm level.

  • [1] Extensive review of GHG mitigation strategies from livestock production:'Mitigation of Greenhouse gas emissions in livestock production - FAO Animal
  • [2] Extensive review of GHG mitigation strategies from livestock production:'Mitigation of Greenhouse gas emissions in livestock production - FAO Animal
  • [3] Extensive review of GHG mitigation strategies from livestock production:'Mitigation of Greenhouse gas emissions in livestock production - FAO Animal
  • [4] Extensive review of GHG mitigation strategies from livestock production:'Mitigation of Greenhouse gas emissions in livestock production - FAO Animal
  • [5] Extensive review of GHG mitigation strategies from livestock production:'Mitigation of Greenhouse gas emissions in livestock production - FAO Animal
 
Source
< Prev   CONTENTS   Source   Next >