Methanogens and Methanogenesis in the Gut: So What and Who Cares?

Herbivorous animals evolved to survive on plant materials rich in cellulose and heteroxylans (hereafter referred to as fiber), and the first step of the process is fiber hydrolysis, which is coordinated by a suite of enzymes including glycoside hydrolases (cellulases and xylanases), esterases, lipases, and proteinases. Once fiber is broken down and deconstructed, the second step of the process is fermentation, which produces acids such as formate, acetate, propionate, butyrate, and succinate as well as ammonia, carbon dioxide, and hydrogen (H2). The short-chain fatty acids (SCFA) and microbial biomass arising from these fermentations can provide the host animal with energyand protein-yielding nutrients, respectively. For humans, these processes are also key, not just for the provision of nutrients (e.g., butyrate for gut epithelial cell metabolism, and the biosynthesis of vitamins), but also for priming the immune system and maintaining the structural integrity of the gut as well as protecting the host from pathogens (Grenham et al., 2011). However, for these two steps to proceed effectively, the hydrogen partial pressure ([H2]) must be kept low because its accumulation can inhibit the most efficient (and ATP-yielding) pathways of fermentation. Although eructation and flatulence do play a role in gas disposal, specific members of the gut microbiota also serve as an important “sink” for H2 consumption. In ruminant livestock, methane production (methanogenesis) serves as a principal route of hydrogen disposal. Although a diversity of individual anaerobic microbes have long been recognized to consume gaseous H2 for the formation of end products such as sulfide and acetic acid, Bryant and Wolin were the first to elucidate some of the cross-feeding (syntrophic) associations between microbes that maintain low [H2] in anaerobic microbial communities, and the term interspecies hydrogen transfer was coined to describe them (Bryant and Wolin, 1975). Interspecies hydrogen transfer is now widely recognized as a critical process underpinning the anaerobic digestion of plant biomass in nature, and in domesticated livestock, as well as environments with limiting amounts of sulfate (e.g., most sources of fresh water) where methaneproducing microbes (methanogens) serve as principal consumers of H2. Although methane emissions during ruminant feed digestion can account for ~10% of the carbon equivalents derived from the feed base being “lost” from the system, it is the perceived environmental impacts of methane emissions from livestock, and their waste, which have fueled the research during the last decade to curb methane emissions from livestock. For instance, various studies have reported that the global annual methane production ranges from 500 to 600 Tg (trillion grams), and as much as 20% of these emissions are attributed to ruminant livestock (Lowe, 2006), but the global demand for meat and milk is also predicted to increase by 60% before 2050 (FAO, 2012). Australia has been identified as one of the world’s largest producers of greenhouse gases on a per-capita basis (Garnaut, 2008), and methane emissions from ruminant livestock are again targeted as a critical control point. There is an increased focus on the development of novel approaches and technologies to manage livestock methane emissions. In relation to human health, breath methane measurements have long been attributed to methanogenic activity in the large bowel. Native African subjects are generally found to possess a higher incidence of methane excretion (~85%) than “Western” European or North American subjects (~50%, as cited by Nava et al., 2012). Methane excretion in Western subjects has been linked with the severity of the constipation symptoms experienced by persons suffering from irritable bowel syndrome (IBS, e.g., Chatterjee et al., 2007) which is a functional disorder now prevalent in Western Methane matters: from blue-tinged moos, to boozy roos, and the health of humans too