‘Commensal’ originates from the Latin word ‘commensalis’ (‘eating at the same table’) and was introduced by Pierre–Joseph van Beneden in 1876. In ecology, the term defines a relationship between two organisms, where one, the commensal, benefits without affecting the other. Thus, commensalism defines a one-way interaction. Originally, the term was used in a host-centric view for interactions where a ‘small’ species (for example, a microorganism) is provided with a habitat (for example, skin) or waste products (for example, methanol released by plants during their cell-wall metabolism (Fall and Benson, 1996)) as food by another, usually much larger host (for example, a mammal or a plant). However, the term commensal has now started to rather imply an unknown, benign function than a truly proven commensal, mutualistic, or antagonistic lifestyle (Casadevall and Pirofski, 2014). In particular when considering interactions among microorganisms, it seems unlikely that a true commensal microorganism exists. It may thus be prudent to assume a function for any kind of microorganism and to reserve commensal for organisms that have been shown not to influence their interaction partner. To emphasise such a microbe-centric view and to imply functionality, we suggest the term tritagonist.
The term tritagonist is adopted from classic drama. In early forms of ancient Greek dramas, only two actors, the protagonist and the deuteragonist, played on stage. The inclusion of a third actor, the tritagonist, allowed for more lifelike and intricate characters and stories. Here, we propose tritagonist as an ecological term for all organisms that influences the interaction between two organisms in a system. Just as in drama, the ecological concept of the tritagonist is meant to promote a better understanding of natural systems. In research, it implies the need to extend oversimplified binary interactions (for example, host–pathogen and pathogen–antagonist pairs) by including additional interaction partners, tritagonists, to obtain a more realistic view of microbial systems (Figure 1a). We advocate the term tritagonist in particular with regard to the recent sequencing efforts in microbiome research, which have revealed a plethora of uncharacterised species and thus laid the foundation to link the evolutionary and genetic diversity with biological functions (Wu et al., 2009; Bulgarelli et al., 2013; Rinke et al., 2013; Panke-Buisse et al., 2015). The in-depth sequence-based knowledge about the microbial species composition of various habitats and of individual strains is in stark contrast to the sparse experimental proof about the biological roles of the identified organisms. In most cases, only a few pathogenic, beneficial or antagonistic interactions are known, while the ecosystem services of the majority of species are unknown. We propose the tritagonist concept to define species with uncharacterised ecological functions to incentivise research on these organisms. The term implies biologically relevant, but yet uncharacterised functions of an organism or groups of organisms, while at the same time leaving room for the exact nature of these functions.
Tritagonists interfere with any other kind of interspecific interaction that may for example be mediated by the following: direct physical interaction, exchange of signalling molecules, nutrient competition, metabolising of by-products, environmental changes (for example, pH) or modulation of host-immune responses (Peleg et al., 2010). Interactions via the environment also take place in time when tritagonists change their resource availability or alter environmental stresses during microbial succession (Fierer et al., 2010). Well-known and medically relevant tritagonists are individual strains used as probiotics or faecal transplantation communities for the treatment of Clostridium difficile infections or other gastrointestinal tract diseases (Gareau et al., 2010; Borody and Khoruts, 2012; Figure 1b). A more specific example for host protection by tritagonists is Bacillus subtilis GS67 that protects Caenorhabditis elegans against Gram-positive pathogens by producing the antibiotic-like substance fengycin in the intestine of the nematode (Iatsenko et al., 2014). A case where tritagonists might reveal new antibiotics are combinations of bacterial species that do not suppress Escherichia coli or Staphylococcus aureus when tested alone, but effectively suppress the human pathogens when co-cultured (Tyc et al., 2014; Figure 1c). Similar concepts as in medical microbiology are pursued in the realm of agricultural microbiology, where single species or combinations of microorganisms are studied and used to control plant pathogens and postharvest diseases, improve the nutrition and resistance of crop plants, or manage the soil, root and plant microbiome (Janisiewicz and Korsten, 2002; Lugtenberg and Kamilova, 2009; Andrews et al., 2012). In a benign type of interaction, yeast species that are associated with arbuscular mycorrhizal fungi improve mycorrhization and benefit plant growth (Boby et al., 2008). However, tritagonists do not always function synergistically, or at least additively, and the biological functions of individual species may alter when the microbial system or the environment changes. For example, combinations of Pseudomonas fluorescens A506 and Pantoea vagans C9-1, which are both individually used as antagonists against Erwinia amylovora, the causal agent of fire blight on Rosaceae (for example, apples, pears), result in reduced fire blight control when co-applied (Stockwell et al., 2011). An intricate tritagonistic interaction between the zygomycete fungus Rhizopus microsporus and Burkholderia rhizoxinica endosymbionts, which produce the potent toxin rhizoxin, results in rice seedling blight (Partida-Martinez and Hertweck, 2005; Figure 1d). These specific examples document the applicability of the tritagonist concept and the value of studying multi-species interactions to broaden our understanding of biological systems.
In summary, we are convinced that describing and studying yet uncharacterised microorganisms as tritagonists will greatly benefit medicine and human physiology, basic research in microbial ecology and applications in agriculture. The term tritagonist shifts the emphasis from the fact that no function is yet known to the a priori assumption that a function must exist and may thus help restoring the proper usage of the term commensal. Tritagonist serves as a name for all the microbial species of a biological system we could ever want to identify and characterise: those that regulate, balance and interfere with microbial interactions without being the most noteworthy players themselves. The concept of the tritagonist will thus, hopefully, stimulate hypothesis-driven research and introduce a systems-biological view of the functional microbiological networks at play in the environment and in hosts.
References
Andrews M, Cripps MG, Edwards GR . (2012). The potential of beneficial microorganisms in agricultural systems. Ann Appl Biol 160: 1–5.
Beneden . (1876) Animal Parasites and Messmates. D. Appleton and Co.: : New York, NY, USA.
Boby VU, Balakrishna AN, Bagyaraj DJ . (2008). Interaction between Glomus mosseae and soil yeasts on growth and nutrition of cowpea. Microbiol Res 163: 693–700.
Borody TJ, Khoruts A . (2012). Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 9: 88–96.
Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P . (2013). Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64: 807–838.
Casadevall A, Pirofski LA . (2014). Microbiology: ditch the term pathogen. Nature 516: 165–166.
Fall R, Benson AA . (1996). Leaf methanol—the simplest natural product from plants. Trends Plant Sci 1: 296–301.
Fierer N, Nemergut D, Knight R, Craine JM . (2010). Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161: 635–642.
Gareau MG, Sherman PM, Walker WA . (2010). Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7: 503–514.
Iatsenko I, Yim JJ, Schroeder FC, Sommer RJ . (2014). B subtilis GS67 protects C. elegans from Gram-positive pathogens via fengycin-mediated microbial antagonism. Curr Biol 24: 2720–2727.
Janisiewicz WJ, Korsten L . (2002). Biological control of postharvest diseases of fruits. Annu Rev Phytopathol 40: 411–441.
Lugtenberg B, Kamilova F . (2009). Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63: 541–556.
Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J . (2015). Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9: 980–989.
Partida-Martinez LP, Hertweck C . (2005). Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437: 884–888.
Peleg AY, Hogan DA, Mylonakis E . (2010). Medically important bacterial-fungal interactions. Nat Rev Microbiol 8: 340–349.
Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF et al. (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499: 431–437.
Stockwell VO, Johnson KB, Sugar D, Loper JE . (2011). Mechanistically compatible mixtures of bacterial antagonists improve biological control of fire blight of pear. Phytopathology 101: 113–123.
Tyc O, van den Berg M, Gerards S, van Veen JA, Raaijmakers JM, de Boer W et al. (2014). Impact of interspecific interactions on antimicrobial activity among soil bacteria. Front Microbiol 5: 567.
Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN et al. (2009). A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056–1060.
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Freimoser, F., Pelludat, C. & Remus-Emsermann, M. Tritagonist as a new term for uncharacterised microorganisms in environmental systems. ISME J 10, 1–3 (2016). https://doi.org/10.1038/ismej.2015.92
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DOI: https://doi.org/10.1038/ismej.2015.92
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