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A major unresolved question in the origin of life is whether there exists a continuous path from geochemical precursors to the majority of molecules in the biosphere, due in part to the autocatalytic nature of metabolic networks in modern-day organisms and high rates of extinction throughout Earth’s history. Here we simulated the emergence of ancient metabolic networks to identify a feasible path from simple geochemical precursors (e.g., phosphate, sulfide, ammonia, simple carboxylic acids, and metals) to contemporary biochemistry, using only known biochemical reactions and models of primitive coenzymes. We find that purine synthesis constitutes a bottleneck for metabolic expansion, and that non-autocatalytic phosphoryl coupling agents are sufficient to enable expansion from geochemistry to modern metabolic networks. Our model predicts distinct phases of metabolic evolution, characterized by the sequential emergence of key molecules (carboxylic acids, amino acids, sugars), purines/nucleotide cofactors (ATP, NAD⁺), flavins, and quinones, respectively. Early phases in the resulting expansion are associated with enzymes that are metal-dependent and structurally symmetric, consistent with models of early biochemical evolution. The production of quinones in the last phase of metabolic expansion permits oxygenic photosynthesis and the production of O₂, leading to a >30% increase in biomolecules. These results reveal a feasible trajectory from simple geochemical precursors to the vast majority of core biochemistry.

Accurate determination of the evolutionary relationships between genes is a foundational challenge in biology. Homology—evolutionary relatedness—is in many cases readily determined based on sequence similarity analysis. By contrast, whether or not two genes directly descended from a common ancestor by a speciation event (orthologs) or duplication event (paralogs) is more challenging, yet provides critical information on the history of a gene. Since 2009, this task has been the focus of the Quest for Orthologs (QFO) Consortium. The sixth QFO meeting took place in Okazaki, Japan in conjunction with the 67th National Institute for Basic Biology conference. Here, we report recent advances, applications, and oncoming challenges that were discussed during the conference. Steady progress has been made toward standardization and scalability of new and existing tools. A feature of the conference was the presentation of a panel of accessible tools for phylogenetic profiling and several developments to bring orthology beyond the gene unit—from domains to networks. This meeting brought into light several challenges to come: leveraging orthology computations to get the most of the incoming avalanche of genomic data, integrating orthology from domain to biological network levels, building better gene models, and adapting orthology approaches to the broad evolutionary and genomic diversity recognized in different forms of life and viruses.

Accurate determination of the evolutionary relationships between genes is a foundational challenge in biology. Homology—evolutionary relatedness—is in many cases readily determined based on sequence similarity analysis. By contrast, whether or not two genes directly descended from a common ancestor by a speciation event (orthologs) or duplication event (paralogs) is more challenging, yet provides critical information on the history of a gene. Since 2009, this task has been the focus of the Quest for Orthologs (QFO) Consortium. The sixth QFO meeting took place in Okazaki, Japan in conjunction with the 67th National Institute for Basic Biology conference. Here, we report recent advances, applications, and oncoming challenges that were discussed during the conference. Steady progress has been made toward standardization and scalability of new and existing tools. A feature of the conference was the presentation of a panel of accessible tools for phylogenetic profiling and several developments to bring orthology beyond the gene unit—from domains to networks. This meeting brought into light several challenges to come: leveraging orthology computations to get the most of the incoming avalanche of genomic data, integrating orthology from domain to biological network levels, building better gene models, and adapting orthology approaches to the broad evolutionary and genomic diversity recognized in different forms of life and viruses., We thank the National Institute for Basic Biology, the Japanese Society for Bioinformatics and the Daiko Foundation for supporting the 67th NIBB Conference/The 6th Quest for Orthologs Meeting. We wish to acknowledge the following support for attending the meetings and/or writing this manuscript: EMBO Young Investigator meeting grant (to C.D.). Service and Infrastructure grant from the Swiss Institute of Bioinformatics, Swiss National Science Foundation [183723] (to C.D.); IdEX Unistra in the framework of the Investments for the future program of the French government (to O.L. and Y.N.); NSF (Award No. 1724300), KAKENHI (Grant No. JP18H01325) (to S.E.M.); support by the research funding program Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz (LOEWE) of the State of Hessen, Research Center for Translational Biodiversity Genomics (TBG) (to I.E.); funding from the Wellcome Trust (108749/Z/15/Z) and the European Molecular Biology Laboratory (to M.P.); National Human Genome Research Institute, National Institutes of Health NIH (grant no. U41HG002273), National Science Foundation NSF (award no. 1917302) (to P.D.T.); Japan Society for the Promotion of Science (16H06279 and 19F19089) (to W.I. and S.C.)., Peer Reviewed, "Article signat per 14 autors/es: Benjamin Linard, Ingo Ebersberger, Shawn E McGlynn, Natasha Glover, Tomohiro Mochizuki, Mateus Patricio, Odile Lecompte, Yannis Nevers, Paul D Thomas, Toni Gabaldón, Erik Sonnhammer, Christophe Dessimoz, Ikuo Uchiyama, QFO Consortium" "Members of the Quest for Orthologs (QFO) Consortium: Adrian Altenhoff, Aida Ouangraoua, Alex Warwick Vesztrocy, Benjamin Linard, Christophe Dessimoz, Damian Szklarczyk, Dannie Durand, David Emms, David Moi, David Thybert, Erik Sonnhammer, Evgenia Kriventseva, Haiming Tang, Hirokazu Chiba, Ikuo Uchiyama, Ingo Ebersberger, Jaime Huerta-Cepas, Jesualdo Tomas Fernandez-Breis, Judith A. Blake, Leszek Pryszcz, Maria-Jesus Martin, Marina Marcet Houben, Mateus Patricio, Matthieu Muffato, Natasha Glover, Odile Lecompte, Paul D. Thomas, Philipp Schiffer, Salvador Capella-Gutierrez, Salvatore Cosentino, Shawn E McGlynn, Shigehiro Kuraku, Sofia Forslund, Steven Kelly, Suzanna Lewis, Tamsin Jones, Tarcisio Mendes de Farias, Taro Maeda, Toni Gabaldon, Wataru Iwasaki, William Pearson, Yan Wang, Yannis Nevers, Yuichiro Hara. All members acknowledged and gave their approval to the content of this manuscript.", Postprint (published version)

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McGlynn, S. E., Glass, J. B., Johnson-Finn, K., Klein, F., Sanden, S. A., Schrenk, M. O., Ueno, Y., & Vitale-Brovarone, A. Hydrogenation reactions of carbon on Earth: linking methane, margarine, and life. American Mineralogist, 105(5), (2020): 599-608, doi:10.2138/am-2020-6928CCBYNCND., Hydrogenation reactions are a major route of electron and proton flow on Earth. Interfacing geology and organic chemistry, hydrogenations occupy pivotal points in the Earth’s global geochemical cycles. Some examples of hydrogenation reactions on Earth today include the production and consumption of methane in both abiotic and biotic reactions, the reduction of protons in hydrothermal settings, and the biological synthesis and degradation of fatty acids. Hydrogenation reactions were likely important for prebiotic chemistry on the early Earth, and today serve as one of the fundamental reaction classes that enable cellular life to construct biomolecules. An understanding and awareness of hydrogenation reactions is helpful for comprehending the larger web of molecular and material inter-conversions on our planet. In this brief review we detail some important hydrogenation and dehydrogenation reactions as they relate to geology, biology, industry, and atmospheric chemistry. Such reactions have implications ranging from the suite of reactions on early Earth to industrial applications like the production of hydrocarbon fuel., S.E.M. is supported by NSF Award 1724300 and JSPS KAKENHI Grant JP18H01325. A.V.B. is supported by ANR T-ERC, CNRS INSU-SYSTER, and Rita Levi Montalcini by MIUR. J.B.G. is supported by NASA Exobiology Grant NNX14AJ87G and 80NSSC19K0477. F.K. is supported by NSF-OCE award 1634032 and 1427274. M.O.S. is supported by the NASA Astrobiology Institute Rock-Powered Life Grant NNA15BB02A.

Recent genomic and microcosm based studies revealed a wide diversity of previously unknown microbial processes involved in alkane and methane metabolism. Here we described a new bacterial genome from a member of the Chloroflexi phylum—termed here Candidatus Chlorolinea photoalkanotrophicum—with cooccurring pathways for phototrophy and the oxidation of methane and/or other small alkanes. Recovered as a metagenome-assembled genome from microbial mats in an iron-rich hot spring in Japan, Ca. ‘C. photoalkanotrophicum’ forms a new lineage within the Chloroflexi phylum and expands the known metabolic diversity of this already diverse clade. Ca. ‘C. photoalkanotrophicum’ appears to be metabolically versatile, capable of phototrophy (via a Type 2 reaction center), aerobic respiration, nitrite reduction, oxidation of carbon monoxide, oxidation and incorporation of carbon from methane and/or other short-chain alkanes such as propane, and potentially carbon fixation via a novel pathway composed of hybridized components of the serine cycle and the 3-hydroxypropionate bi-cycle. The biochemical network of this organism is constructed from components from multiple organisms and pathways, further demonstrating the modular nature of metabolic machinery and the ecological and evolutionary importance of horizontal gene transfer in the establishment of novel pathways.

Biological methane cycling plays an important role in Earth's climate and the global carbon cycle, with biological methane oxidation (methanotrophy) modulating methane release from numerous environments including soils, sediments, and water columns. Methanotrophy is typically coupled to aerobic respiration or anaerobically via the reduction of sulfate, nitrate, or metal oxides, and while the possibility of coupling methane oxidation to phototrophy (photomethanotrophy) has been proposed, no organism has ever been described that is capable of this metabolism. Here we described a new bacterial genome from a member of the Chloroflexi phylum--termed here Candidatus Chlorolinea photomethanotrophicum--with cooccurring methanotrophy and phototrophy pathways, suggesting a novel link between these two metabolisms. Recovered as a metagenome-assembled genome from microbial mats in an iron-rich hot spring in Japan, Ca. "C. photomethanotrophicum" forms a new lineage within the Chloroflexi phylum and expands the known metabolic diversity of this already diverse clade. Ca. "C. photomethanotrophicum" appears to be metabolically versatile, capable of phototrophy (via a Type 2 reaction center), aerobic respiration, nitrite reduction, oxidation of methane and carbon monoxide, and potentially carbon fixation via a novel pathway composed of hybridized components of the serine cycle and the 3-hydroxypropionate bicycle. The biochemical network of this organism is constructed from components from multiple organisms and pathways, further demonstrating the modular nature of metabolic machinery and the ecological and evolutionary importance of horizontal gene transfer in the establishment of novel pathways.