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bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Sulfur reduction coupling with anaerobic ammonium oxidation drives proto-anabolic 2 networks 3 Peng Bao1, 2, *, Guo-Xiang Li1, 2, 3, Hu Li1 4 5 1Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese 6 Academy of Sciences, Xiamen 361021, P. R. China 7 2Ningbo Urban Environment Observation and Station, Chinese Academy of Sciences, 8 Ningbo 315800, P. R. China 9 3University of Chinese Academy of Sciences, Beijing 100049, P. R. China 10 11 Address correspondence to: 12 Dr. Peng Bao 13 Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, P. R. 14 China 15 E-mail: [email protected]; [email protected] 16 17 18 bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 19 Abstract 20 The geochemical energy that drives the transition from non-life to life is as yet 21 unknown. Here we show that thiosulfate/sulfate reduction coupling with anaerobic 22 ammonium oxidation (Sammox), could provide the primordial redox equivalents and 23 energy for prebiotic proto-anabolic networks, the reductive acetyl-CoA pathway 24 combined with incomplete reductive tricarboxylic acid (rTCA) cycle, reductive 25 amination and pyrrole synthesis. Fe-S mineral catalysis and thiols/thioesters as energy 26 couplers enhance the efficiency of prebiotic proto-anabolic networks in 27 thiosulfate-fueled Sammox reaction systems under hydrothermal conditions. Results 28 implied that thiosulfate-fueled Sammox should be the primordial reaction driving the 29 construction of proto-anabolic networks rather than sulfate-fueled Sammox, as it 30 could be catalyzed, and also sulfate would have been severely limiting in ancient 31 oceans. To confirm our findings, we isolated and identified a mixtrophic Sammox 32 bacterium, Ralstonia thioammoniphilus GX3-BWBA, which prefer thiosulfate to 33 sulfate. Genomic analysis of R. thioammoniphilus GX3-BWBA implied that this 34 ancient metabolism in modern microbes should contain two stages according to 35 ammonium transformation, —oxidation of ammonium to nitrite and denitrification. 36 The incomplete rTCA cycle and reductive acetyl-CoA pathway were all identified in 37 R. thioammoniphilus GX3-BWBA metabolic networks, which were responsible for 38 chemolithotrophic metabolism. We inferred that Sammox drove the coupling of the 39 biochemical transformation of C, H, O, N, S, and/or Fe simultaneously in Hadean 40 alkaline hydrothermal systems, thereby permitting the emergence of life. The results bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 41 bridged the gap in the transition from geochemistry to biochemistry. 42 43 bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 44 The transition from non-life to life occurred in the context of geochemical energy 45 derived from element-coupled transformation1-3. The chemistry of life is based on 46 redox reactions, that is, successive transfers of electrons and protons from the six 1,4 47 major elements, i.e., C, H, O, N, S, and P . The H2/CO2 redox couple, which can 48 occur in submarine hydrothermal vents, has been proposed to drive the reductive 49 acetyl-CoA pathway, an ancient metabolic route3,5-7. Nevertheless, the primordial 50 energy source of the H2/CO2 redox couple suffers from the difficulty that the 8 51 exergonic reaction competes with the endergonic reaction for available H2 . The 52 subsequent surface metabolism and thioester world theories still could not answer the 53 question, how the required reduced carbon compounds have been synthesized9,10. 54 Despite this limitation, these theories have emphasized the important roles of 55 thioesters and Fe-S mineral catalysis for driving the primordial rTCA cycle, a central 56 anabolic biochemical pathway whose origins are proposed to trace back to 57 geochemistry9,11,12. 58 Native iron/metals were recently shown to promote the reductive acetyl-CoA 59 pathway and rTCA cycle and strongly support the feasibility of these two primordial 60 synthetic pathways13,14, although they were generally considered to be rare near the 61 Earth’s surface13 and cannot support the long elemental transition from geochemistry 62 to biochemistry. Proto-anabolic networks consisting of the reductive acetyl-CoA 63 pathway together with the complete/incomplete rTCA cycle as primordial synthetic 64 pathways are therefore more logical3,15-18. However, the initial driving force for the 65 rise of proto-anabolic networks is still unclear. Moreover, the roles of N and S bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 66 geochemical transformation in the origin of life have been largely ignored because 67 computational analysis has implied that N and S are essential for thermodynamically 68 feasible phosphate-independent metabolism before the rise of last universal common 69 ancestor (LUCA)19. The proto-anabolic networks might be driven by C, H, O, N, S, 70 and/or Fe coupling transformation at their earliest stage of the transition from 71 geochemistry to biochemistry. The co-evolution of the metabolism of those elements 72 may provide strong explanatory power for the origin of life and explain why the 73 structure of metabolic networks is as it is. We therefore speculate that 74 thermodynamically feasible sulfurous species reduction coupling with anaerobic 75 ammonium oxidation reaction20,21,22,23,24 (Eqs. 1, 2; pH=8.0), with/without the 76 catalysis of Fe-S minerals and thioesters, may have been the primordial power force 77 for the rise of proto-anabolic networks. 78 8NH+2-- +2SO +2HCO→ 4N +2HS - +CH COO - +12H O+5H +∆G = -20.0 kJ mol-1 44 3 2 3 2 r (1) 79 4NH+2-- +S O +2HCO→ 2N +2HS- +2HCOO - +5H O+4H +∆G = -13.4 kJ mol-1 (2) 423 3 2 2 r 80 On early Earth, elemental sulfur, sulfite, and thiosulfate were produced 81 abundantly from volcanic and hydrothermal SO2 or from H2S oxidation by iron oxides 82 in sulfide-rich hydrothermal fluid2,15,25. In simulated hydrothermal systems with 26 83 conditions of 300 °C and high pressure, nitrite was readily converted to NH3 , and 84 Ni-Fe metals and alloys were also effective catalysts of N2 reduction to NH3 in 27 85 Hadean hydrothermal systems . There would have been much higher CO2 86 concentrations in the oceans on early Earth because there was perhaps up to 1000 28 87 times more CO2 in the atmosphere than that today . bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 88 Hence, when sulfurous species and NH3 in Hadean hydrothermal systems made 89 contact with CO2, there were spontaneous electron and proton transfers for energy 90 generation and organic molecule synthesis via sulfurous species reduction coupling 91 with ammonium oxidation. As sulfate would have been severely limiting in ancient 92 oceans2,29, we termed this process Sammox, and a Sammox microbe is more likely 93 use thiosulfate, elemental sulfur and sulfite as electron acceptor besides sulfate, 94 distinguishing it from previous studies of the coupling elemental biogeochemical 95 cycles1,30. A prebiotic reaction should occur with the ability to branch out into S and 96 N biochemistry, which could contribute to the autocatalysis and evolution of 97 primordial metabolic networks. Thus, Sammox may facilitate the synthesis of 98 thioesters and amino acids, which are essential for the self-amplification of 99 phosphate-independent metabolic networks before the rise of LUCA. We expect that 100 prebiotic chemical evidence of Sammox-powered CO2 fixation, thioesters, amino acid 101 and co-factors synthesis, combined with genetic analysis of a representative Sammox 102 microbe, will provide profound insights into the earliest origins of life and fill in the 103 missing link of the emergence of biochemistry from geochemistry. 104 105 Results and discussion 106 Sammox drives the combination of abiotic reductive acetyl-CoA pathway and 107 incomplete rTCA cycle 108 First, we aimed to verify the feasibility of Sammox-driven abiotic reductive 109 acetyl-CoA pathway, rTCA cycle, and off-cycle reactions (reductive amination and bioRxiv preprint doi: https://doi.org/10.1101/461707; this version posted January 30, 2019.