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Archaea, specific genetic traits, and development of improved bacterial live biotherapeutic products: another face of next-generation probiotics

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Abstract

Trimethylamine (TMA) and its oxide TMAO are important biomolecules involved in disease-associated processes in humans (e.g., trimethylaminuria and cardiovascular diseases). TMAO in plasma (pTMAO) stems from intestinal TMA, which is formed from various components of the diet in a complex interplay between diet, gut microbiota, and the human host. Most approaches to prevent the occurrence of such deleterious molecules focus on actions to interfere with gut microbiota metabolism to limit the synthesis of TMA. Some human gut archaea however use TMA as terminal electron acceptor for producing methane, thus indicating that intestinal TMA does not accumulate in some human subjects. Therefore, a rational alternative approach is to eliminate neo-synthesized intestinal TMA. This can be achieved through bioremediation of TMA by these peculiar methanogenic archaea, either by stimulating or providing them, leading to a novel kind of next-generation probiotics referred to as archaebiotics. Finally, specific components which are involved in this archaeal metabolism could also be used as intestinal TMA sequesters, facilitating TMA excretion along with stool. Referring to a standard pharmacological approach, these TMA traps could be synthesized ex vivo and then delivered into the human gut. Another approach is the engineering of known probiotic strain in order to metabolize TMA, i.e., live engineered biotherapeutic products. These alternatives would require, however, to take into account the necessity of synthesizing the 22nd amino acid pyrrolysine, i.e., some specificities of the genetics of TMA-consuming archaea. Here, we present an overview of these different strategies and recent advances in the field that will sustain such biotechnological developments.

Key points

• Some autochthonous human archaea can use TMA for their essential metabolism, a methyl-dependent hydrogenotrophic methanogenesis.

• They could therefore be used as next-generation probiotics for preventing some human diseases, especially cardiovascular diseases and trimethylaminuria.

• Their genetic capacities can also be used to design live recombinant biotherapeutic products.

• Encoding of the 22nd amino acid pyrrolysine is necessary for such alternative developments.

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Funding

JFB is supported by a grant from the Agence Nationale de la Recherche of the French government through the program “Investissements d’Avenir” (16-IDEX-0001 CAP 20–25), through an “Innovation-Research” grant from Hub Innovergne. Work in PWOT’s lab is supported by an award from Science Foundation Ireland to APC Microbiome Ireland.

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Author notes

  1. Marie-Edith Arnal

    Present address: CEA, CNRS, IRIG, SyMMES, Chimie Interface Biologie pour l’Environnement, la Santé et la Toxicologie (CIBEST), Univ. Grenoble Alpes, F-38000, Grenoble, France

Authors and Affiliations

  1. CNRS, Laboratoire Microorganismes: Génome et Environnement LMGE, Université Clermont Auvergne, F-63000, Clermont-Ferrand, France

    Khaled Fadhlaoui, Marie-Edith Arnal, Matthieu Martineau, Paméla Camponova & Jean-François Brugère

  2. Aix Marseille Université, CNRS, Université de Toulon, IRD, Mediterranean Institute of Oceanography (MIO), Marseille, France

    Bernard Ollivier

  3. School of Microbiology and APC Microbiome Ireland, University College Cork, Cork, Ireland

    Paul W. O’Toole

Authors
  1. Khaled Fadhlaoui
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  2. Marie-Edith Arnal
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  3. Matthieu Martineau
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  4. Paméla Camponova
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  7. Jean-François Brugère
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Contributions

JFB and PWOT are inventors on patent WO2014082773A1 co-owned by their respective universities. PWOT is a founder of 4D Pharma Cork Ltd., a role that has not constrained or influenced this review. All the authors contributed to the written of the manuscript and the conception and design of figures. All the authors read and approved the manuscript.

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Correspondence to Jean-François Brugère.

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Fadhlaoui, K., Arnal, ME., Martineau, M. et al. Archaea, specific genetic traits, and development of improved bacterial live biotherapeutic products: another face of next-generation probiotics. Appl Microbiol Biotechnol 104, 4705–4716 (2020). https://doi.org/10.1007/s00253-020-10599-8

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