Microbial syntrophy: interaction for the common good

Abstract

Classical definitions of syntrophy focus on a process, performed through metabolic interaction between dependent microbial partners, such as the degradation of complex organic compounds under anoxic conditions. However, examples from past and current scientific discoveries suggest that a new, simple but wider definition is necessary to cover all aspects of microbial syntrophy. We suggest the term 'obligately mutualistic metabolism', which still focuses on microbial metabolic cooperation but also includes an ecological aspect: the benefit for both partners. By the combined metabolic activity of microorganisms, endergonic reactions can become exergonic through the efficient removal of products and therefore enable a microbial community to survive with minimal energy resources. Here, we explain the principles of classical and non-classical syntrophy and illustrate the concepts with various examples. We present biochemical fundamentals that allow microorganism to survive under a range of environmental conditions and to drive important biogeochemical processes. Novel technologies have contributed to the understanding of syntrophic relationships in cultured and uncultured systems. Recent research highlights that obligately mutualistic metabolism is not limited to certain metabolic pathways nor to certain environments or microorganisms. This beneficial microbial interaction is not restricted to the transfer of reducing agents such as hydrogen or formate, but can also involve the exchange of organic, sulfurous- and nitrogenous compounds or the removal of toxic compounds.

Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

“…As a consequence, the resulting consortia can exploit new ecological niches that were inaccessible to the individual genotypes before entering into the synthrophic interaction (Morris et al, 2013), thus allowing them to escape competition with conspecifics.…”

“…As amino-acid overproduction incurred significant fitness costs (Figure 2b), genotypes that take advantage of the released 'public good' without reciprocating are selectively favoured and thus expected to exploit the resource until the ecological interaction collapses (Axelrod and Hamilton, 1981;Bull and Rice, 1991;Sachs et al, 2004). Nevertheless, obligate mutualisms are widespread in nature among both micro- (Schink, 2002;Morris et al, 2013) and macroorganisms (Boucher, 1988;Douglas, 1994) and, in some of these cases, noncooperating types have been described to coexist with mutualists for extended evolutionary periods (Sachs and Simms, 2006). It is generally believed that either derived 'partner choice' mechanisms such as the punishment of non-cooperating individuals (Bull and Rice, 1991;Yu, 2001) or spatially structured environments (Doebeli and Knowlton, 1998;Wilson et al, 2003) are required to protect mutually beneficial interactions from being exploited by non-cooperators.…”

“…This type of cooperative interaction is very widespread among both Bacteria and Archaea and is frequently based on the reciprocal exchange of certain metabolites (Schink, 2002;McInerney et al, 2008;Sieuwerts et al, 2008;Morris et al, 2013). For those cases, where the interaction partners have been studied in more detail, characteristic features such as the loss of essential biosynthetic functions (McInerney et al, 2007) or the formation of physical attachment structures (Ishii et al, 2005;Wanner et al, 2008) have been reported that may have arisen as specific adaptations to the symbiotic lifestyle.…”

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

“…Metabolic interactions between species, such as detoxification of metabolic waste and cross-feeding, shape microbial communities and regulate ecosystem processes (Schink, 2002;Fuhrman, 2009;Morris et al, 2013). Study of these interactions can be encumbered by the stochasticity and complexity of natural systems.…”

H2metabolism is widespread and diverse among human colonic microbes

“…7 Interspecies hydrogen transfer is the syntrophic evolution and consumption of hydrogen between organisms in such close proximity that hydrogen never joins the dissolved hydrogen pool. 8,9 In contrast, competitive hydrogenotrophy pairs the oxidation of organic substrates by hydrogenogens with the reduction of terminal electron acceptors by hydrogenotrophs, which results in a well described ecological framework determined by H 2 concentration and substrate availability. In a substrate-rich environment, competitive advantage is gained by hydrogenotrophs able to reduce substrates at low hydrogen concentrations, as the concentration is maintained too low to make growth thermodynamically favorable for other hydrogenotrophic organisms.…”