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Proposal of the Reverse Flow Model for the Origin of the Eukaryotic Cell Based on Comparative Analyses of Asgard Archaeal Metabolism

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Proposal of the Reverse Flow Model for the Origin of the Eukaryotic Cell Based on Comparative Analyses of Asgard Archaeal Metabolism ARTICLES https://doi.org/10.1038/s41564-019-0406-9 Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism Anja Spang 1,2*, Courtney W. Stairs 1, Nina Dombrowski2,3, Laura Eme 1, Jonathan Lombard1, Eva F. Caceres1, Chris Greening 4, Brett J. Baker3 and Thijs J. G. Ettema 1,5* The origin of eukaryotes represents an unresolved puzzle in evolutionary biology. Current research suggests that eukary- otes evolved from a merger between a host of archaeal descent and an alphaproteobacterial endosymbiont. The discovery of the Asgard archaea, a proposed archaeal superphylum that includes Lokiarchaeota, Thorarchaeota, Odinarchaeota and Heimdallarchaeota suggested to comprise the closest archaeal relatives of eukaryotes, has helped to elucidate the identity of the putative archaeal host. Whereas Lokiarchaeota are assumed to employ a hydrogen-dependent metabolism, little is known about the metabolic potential of other members of the Asgard superphylum. We infer the central metabolic pathways of Asgard archaea using comparative genomics and phylogenetics to be able to refine current models for the origin of eukaryotes. Our analyses indicate that Thorarchaeota and Lokiarchaeota encode proteins necessary for carbon fixation via the Wood–Ljungdahl pathway and for obtaining reducing equivalents from organic substrates. By contrast, Heimdallarchaeum LC2 and LC3 genomes encode enzymes potentially enabling the oxidation of organic substrates using nitrate or oxygen as electron acceptors. The gene repertoire of Heimdallarchaeum AB125 and Odinarchaeum indicates that these organisms can ferment organic substrates and conserve energy by coupling ferredoxin reoxidation to respiratory proton reduction. Altogether, our genome analyses sug- gest that Asgard representatives are primarily organoheterotrophs with variable capacity for hydrogen consumption and pro- duction. On this basis, we propose the ‘reverse flow model’, an updated symbiogenetic model for the origin of eukaryotes that involves electron or hydrogen flow from an organoheterotrophic archaeal host to a bacterial symbiont. he exploration of microbial life inhabiting anoxic environ- of eukaryotes and about the evolutionary events that led to the ments has changed our perception of microbial diversity, evo- origin of the eukaryotic cell13–16. Even though recent data favour lution and ecology, and unveiled various previously unknown hypotheses that underpin a symbiogenetic origin of eukaryotes T 1 6,8,17,18 branches in the tree of life , including the proposed Asgard archaea from only two domains of life , the timing of the events leading superphylum2–4. The analysis of genomes from uncultivated micro- to eukaryogenesis remains unknown19. organisms has improved our understanding of microbial metabolic Here, we perform a comparative analysis of the metabolic poten- diversity and evolution of life on Earth, including the origin of tial of the Asgard superphylum, which revealed considerable meta- eukaryotes5. During the past years, models that posit that eukary- bolic versatility in these archaea. In light of our findings, we update otes evolved from a symbiosis between an alphaproteobacterial previously formulated symbiogenetic hypotheses and present a endosymbiont and an archaeal host cell have gained increasing refined model for the origin of eukaryotes, in which the archaeal support (reviewed in refs. 6–8). In particular, detailed phylogenomic host is suggested to be a fermentative organoheterotroph generating analyses of Asgard archaea, which currently include Lokiarchaeota, reduced compounds that are metabolized by a syntrophic bacterial Thorarchaeota, Odinarchaeota and Heimdallarchaeota, have sug- partner organism. gested that these archaea represent the closest known relatives of eukaryotes2,4. Although this view has been challenged9, additional Results and discussion analyses supported the phylogenetic placement of eukaryotes Genomic analyses of Asgard archaea reveal different meta- within the Asgard archaea and reinforced the suggestion that these bolic repertoires. Our reconstruction of the metabolism of the organisms are key for our understanding of eukaryogenesis10,11. The Asgard archaea, based on comparative genome annotation and genomes of all members of the Asgard archaea are enriched in genes phylogenetic analyses, revealed that the enzymatic repertoire encoding so-called eukaryotic signature proteins2,4,12, indicating differs both within and between the metagenome-assembled that the elusive archaeal ancestor of eukaryotes already contained genomes (MAGs) of representatives of the Lokiarchaeota, several building blocks for the subsequent evolution of eukary- Thorarchaeota, Odinarchaeota and Heimdallarchaeota4, suggest- otic complexity2,4. In turn, genome analyses of Lokiarchaeum have ing that members of these groups are characterized by different reinvigorated discussions about the nature of the archaeal ancestor physiological lifestyles. 1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden. 2NIOZ, Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, AB Den Burg, The Netherlands. 3Department of Marine Science, University of Texas at Austin, Marine Science Institute, Port Aransas, TX, USA. 4School of Biological Sciences, Monash University, Clayton, Victoria, Australia. 5Laboratory of Microbiology, Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen, The Netherlands. *e-mail: [email protected]; [email protected] 1138 NatURE MICROBIOLOGY | VOL 4 | JULY 2019 | 1138–1148 | www.nature.com/naturemicrobiology NATURE MICROBIOLOGY ARTICLES ? e ? ase se nas e + + H + H + H H + H+ H+ H ive dehalogena ATP synthase ATP synthas ADH dehydroge + N H+ ETFQO? Reductive dehalogenHdrD? H ETFQO? Reduct HdrD? MQ MQ MQ MQ MQ MQ ? MQ ? ? (red) ATP (red) ATP (ox) ? ? ? (red) ETF (ox) (red) NAD + ETF ? ox ? Fd(ox) ox (ox) ADP + P (ox) ADP + P i ETF Fd(red) i NADH ETF Fd red FAD H 3c [NiFe]- red (ox) 2 Fd(red) ? – + hydrogenase 3c [NiFe]- (ox) FADH H FAD H2 Archaeal lipid – Archaeal lipid ? + hydrogenase ? HdrABC linked (ox) FADH H biosynthesis (red) biosynthesis HdrABC linked ? (red) Glucose NADPH H+ 3b [NiFe]- Glucose Ribose-5P NADP H hydrogenase Glycerol-1P + Glycerol-1P 2 NADPH H 3b [NiFe]- . RuMP Non-ox. PPP NADP H hydrogenase s 2 i s rev Ribose-5P i s s Glycerone-P e Glycerone-P e - n n CO HCOO CO 2 e 2 e - Fd g NADH HCOO g NADH red P EM Formate o Fd P EM red o Fd F420 ox CO ox e Ribose-1,5-2P Fd e 2 ox NMP dehydro- n Formate n F420 F420 red o CO CO ox o NADH genase 2 2 dehydro- CO2 c c F420 F420 u red l u CO red CO genase l 2 2 F420red F420ox G G F420ox F420red - F420 Mevalonate F420red Mevalonate β WLP ox - WLP ETF Acetyl-CoA β F420ox Acetyl-CoA oxidation red pathway ETFred pathway NADH NADH oxidation NADH NADH Fumarate Acetyl-CoA Fumarate Acetyl-CoA Succinate TCA TCA dehydrogenase MQ ADP + Pi MQ ADP + P Succinate H+ Succinate i H+ ATP NADH ATP NADH 2Pi PPi + H2O 2Pi PPi + H2O Acetate Acetate Lokiarchaeota Thorarchaeota e ? xidas se e 2 o er e se H+/Na+ e]-hydrogenase H+/Na+ -hydrogena F e] dehalogenase reductas + + + dehydrogenas [Ni + + ynthase H /Na H 4 H /Na s synthase DH + + ochrome/quinol 4 [NiF + + H /Na O Nitrate Haem-copper-type + + e]-hydrogena H /Na NA Type Mrp-like antoport H /Na ATP iF H+/Na+ ATP ? BCP ype + + cyt [N T Mrp-like antiporter+ + ETFQ Reductive H ? H H /Na MQ MQ MQ H+ MQ ? H + ? (red) - H2O 2 H Fd(red) NO + H O ATP + H 2 2 ATP NAD 2 ? (ox) - Fd + Fd ? ETF + O 2P PP + H O (ox) H (red) H Fd ox NO3 + H 2 i + i 2 2 ADP + P NADH (ox) ADP + P H i ETF + i Fd Fd red MQ H (red) (ox) ? ? (ox) HdrD Archaeal lipid ? (red) Archaeal lipid biosynthesis biosynthesis NADPH H+ 3b [NiFe]- Glucose Fd Glucose (ox) NADP H hydrogenase ox. PPP1 Fd 2 Glycerol-1P Ribose-5P (red) 3c [NiFe]- Glycerol-1P FAD H2 1 – ? + hydrogenase rev. RuMP (ox) FADH H rev. RuMP s s i i Ribose-5P Ribose-5P s CO s ? HdrABC linked Glycerone-P (red) 2 Glycerone-P e e Fe n red n e Fe e NADH/Fd (red) ox g g P EM NADPH o P EM o e e NMP NMP n n F420 o CO CO red o + 2 2 CO c F420 c 2 NADPH H 3b [NiFe]- ox u u l F420 l NADP H hydrogenase red 2 G F420 G ox ADP + Pi ATP WLP Mevalonate Mevalonate pathway Acetyl-CoA Acetate pathway Acetyl-CoA NADH NADH NADH Acetyl-CoA Fumarate ETFred Succinate ADP + P TCA TCA i dehydrogenase - MQ Succinate β H+ ATP oxidation 2P PP + H O NADH i i 2 NADH Acetate Heimdallarchaeota Odinarchaeota Present Partial or potentially present Absent Fig. 1 | Metabolic potential of different Asgard phyla. Each of the arrows represent functions that were assigned to predicted proteins encoded in the respective genomes (Lokiarchaeota (two MAGs), Thorarchaeota (three MAGs), Heimdallarchaeota (three MAGs) and Odinarchaeota (one MAG)). 1The oxidative pentose phosphate pathway (ox. PPP) is encoded by Heimdallarchaeum LC2 and LC3, and the reductive ribulose monophosphate (rev. RuMP) pathway by Heimdallarchaeum AB125. 2The location of the active site of nitrate reductase in Asgard homologues is probably in the cytoplasm (Supplementary Information). The colour code as indicated in the figure key is as follows: the black arrows indicate enzymatic steps encoded by the respective organisms; the solid grey arrows indicate enzymatic steps for which either only putative enzymes could be identified or enzymatic steps that are only encoded in some of the representatives of a given phylum; and the dashed grey arrows reveal enzymatic steps for which no (candidate) enzymes could be found in any of the representatives of a particular phylum. The presence or function of enzyme complexes surrounded by the black dashed lines is tentative. ETF, electron transfer flavoprotein; ETFQO, ETF-ubiquinone oxidoreductase; Fd, ferredoxin; HdrD, heterodisulfide reductase; ox, oxidation; P, phosphate; Pi, inorganic phosphate; PPi, inorganic pyrophosphate; red, redox; TCA; tricarboxylic acid cycle.
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