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The Sunlit Microoxic Niche of the Archaeal Eukaryotic Ancestor Comes 2 to Light

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The Sunlit Microoxic Niche of the Archaeal Eukaryotic Ancestor Comes 2 to Light bioRxiv preprint doi: https://doi.org/10.1101/385732; this version posted August 20, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 The sunlit microoxic niche of the archaeal eukaryotic ancestor comes 2 to light 3 4 Paul-Adrian Bulzu1#, Adrian-Ştefan Andrei2#, Michaela M. Salcher3, Maliheh Mehrshad2, 5 Keiichi Inoue5, Hideki Kandori6, Oded Beja4, Rohit Ghai2*, Horia L. Banciu1,7 6 1Department of Molecular Biology and Biotechnology, Faculty of Biology and Geology, Babeş-Bolyai 7 University, Cluj-Napoca, Romania 8 2Institute of Hydrobiology, Department of Aquatic Microbial Ecology, Biology Centre of the Academy 9 of Sciences of the Czech Republic, České Budějovice, Czech Republic. 10 3Limnological Station, Institute of Plant and Microbial Biology, University of Zurich, Seestrasse 187, 11 CH-8802 Kilchberg, Switzerland. 12 4Faculty of Biology, Technion Israel Institute of Technology, Haifa, Israel. 13 5The Institute for Solid State Physics, The University of Tokyo, Kashiwa, Japan 14 6Department of Life Science and Applied Chemistry, Nagoya Institute of Technology, Nagoya, Japan. 15 7Molecular Biology Center, Institute for Interdisciplinary Research in Bio-Nano-Sciences, Babeş- 16 Bolyai University, Cluj-Napoca, Romania 17 18 19 20 21 # These authors contributed equally to this work 22 *Corresponding author: Rohit Ghai 23 Institute of Hydrobiology, Department of Aquatic Microbial Ecology, Biology Centre of the Academy 24 of Sciences of the Czech Republic, Na Sádkách 7, 370 05, České Budějovice, Czech Republic. 25 Phone: +420 387 775 881 26 Fax: +420 385 310 248 27 E-mail: [email protected] 28 29 30 31 32 33 34 35 1 bioRxiv preprint doi: https://doi.org/10.1101/385732; this version posted August 20, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 36 Summary 37 Recent advances in phylogenomic analyses and increased genomic sampling of uncultured 38 prokaryotic lineages brought compelling evidence in support of the emergence of eukaryotes from 39 within the Archaea domain of life. The discovery of Asgardaeota archaea and their recognition as the 40 closest extant relative of eukaryotes fuelled the revival of a decades-old debate regarding the 41 topology of the tree of life. While it is apparent that Asgardaeota encode a plethora of eukaryotic- 42 specific proteins (the highest number identified to date in prokaryotes), the lack of genomic 43 information and metabolic characterization has precluded inferences about their lifestyles and the 44 metabolic landscape that may have favoured the emergence of the hallmark eukaryotic subcellular 45 architecture. Here, we use advanced phylogenetic analyses to infer the deep ancestry of eukaryotes 46 and genome-scale metabolic reconstructions to shed light on the metabolic milieu of the closest 47 archaeal eukaryotic ancestors discovered till date. In doing so, we: i) generate the largest 48 Asgardaeota genomic dataset available so far, ii) describe a new clade of rhodopsins encoded within 49 the recovered genomes, iii) provide unprecedented evidence for mixotrophy within Asgardaeota, iv) 50 present first-ever proofs that the closest extant archaeal relatives to all eukaryotes 51 (Heimdallarchaeia) have microoxic lifestyles with aerobic metabolic pathways unique among 52 Archaea (i.e. kynurenine pathway) and v) generate the first images of Asgardaeota. 53 54 Main 55 At the dawn of genomics, the eukaryotes were recognized as amalgamated genetic jigsaws that bore 56 components of both bacterial and archaeal descent1,2. This genomic chimerism served as a source of 57 speculation and debate over the nature of the protoeukaryote ancestors3–5 and inspirited a plethora 58 of hypothetical scenarios for the processes that led to eukaryogenesis2,6. Even though, in light of 59 recent research, eukaryotes came into existence through the interplay between an archaeal host7 60 and a bacterial endosymbiont8, the metabolic milieu of the ancestral prokaryotic lineages and their 61 phylogenetic blueprint still remain elusive. Here, we bridge state-of-the-art cultivation-independent 62 genomics, sensitive molecular phylogenetic analyses and genome-scale metabolic reconstructions in 63 order to shed light upon the deep archaeal ancestors of eukaryotes, as well as the metabolic 64 landscape that favored the rise of the ‘nucleated cellular architecture’. The genomic catalogue 65 generated during this study enabled us to confidently resolve the backbone of the Asgardaeota 66 superphylum9 (the closest archaeal relatives of eukaryotes described to date) and to narrow down 67 the eukaryotes’ branching point within the tree of life. Collectively, our analyses revealed that 68 contradictory to current opinions10 the archaeal protoeukaryote ancestor was likely microaerophilic 69 and possessed the ability to harness the Sun’s energy via rhodopsins, and whose mixotrophic 70 metabolism had already acquired unprecedented (within archaea) circuitries for de novo aerobic 71 NAD+ synthesis. 72 Asgardaeota phylogenomics: Homology-based searches were employed to recover Asgardaeota- 73 related contigs from de novo metagenomic assemblies of two deep-sequenced lake sediment 74 samples (with contrasting salinities). By utilizing a hybrid binning strategy and performing manual 75 inspection and data curation, we obtained thirty-five Asgardaeota MAGs (metagenome-assembled 76 genomes), spanning three (out of 4) evolutionary lineages within the superphylum: Lokiarchaeia 77 (23), Thorarchaeia (10), and Heimdallarchaeia (2). To the best of our knowledge, by accurately 78 binning 6 026 contigs (total length 55.75 Mbp, average contig length 9 252.5 bp) we generated the 79 largest genomic dataset available to date for this superphylum (in contrast all publicly available 80 MAGs amount to 47.2 Mbp). Due to the challenges associated with reconstructing the evolutionary 81 relationships between archaea and eukayotes9, in our inferences we used only those MAGs (n= 8; 82 Supplementary Table S1) that harbored at least 75% of total phylogenetic markers (See 83 Supplementary Table S3). The maximum-likelihood phylogenetic tree, based on concatenation of 84 small (SSU) and large (LSU) ribosomal RNA genes, pictured for the first time a topology in which 2 bioRxiv preprint doi: https://doi.org/10.1101/385732; this version posted August 20, 2018. 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. 85 eukaryotes branched with high-support from within Asgardaeota (archaea) (Supplementary Figure 86 S1a). Even more remarkably, in addition to recreating a previously described Asgardaeota/Eukaryota 87 branching pattern9, we provide unprecedented support for a close evolutionary linkage between 88 Heimdallarchaeia (Asgardaeota superphylum) and eukaryotes (SH-aLRT=97.5; UFBoot=100) 89 (Supplementary Figure S1a). The genome-focused phylogeny of Asgardaeota revealed a pattern of 90 ancestry, divergence, and descent, in which Heimdallarchaeia comprises the basal branch of the 91 superphylum and Thor-/Odinarchaeia the youngest one (Figure 1a). Although dissimilar in branching 92 pattern with the SSU + LSU tree, the phylogenomic one was found to be robust (Figure 1a) and to 93 support a topology brought into attention by an earlier study9. The SR4-recoded11 Bayesian tree 94 (maxdiff=0.1) resolved with high support (PP=1) the monophyly of Asgardaeota/Eukaryota, but failed 95 to confidently resolve the internal topology of the superphylum and the branching point of 96 eukaryotes (Figure 1b). Noteworthy, in both SR4-recoded Bayesian (Figure 1b) and maximum- 97 likelihood phylogenies (Supplementary Figure S1b) the eukaryotes caused branch instability for 98 Heimdallarchaeia, which was attracted without statistical support within the superphylum (PP=0.52; 99 SH-aLRT=92.4 and UFBoot=88). To further substantiate the phylogenetic connection between 100 Asgardaeota members and eukaryotes, we screened all the recovered MAGs and the publicly 101 available ones (14) for the presence of potential eukaryotic signature proteins (ESP). Similar to 102 previous reports3,9,12, the MAGs were found to be highly enriched with ESP (Figure 1c), which further 103 reinforced their ancestral linkage to eukaryotes. In addition to the reported ESP9, we identified a 104 potential subunit of the COPII vesicle coat complex (associated with intracellular vesicle traffic and 105 secretion) in Thorarchaeia and proteins that harbor the N-terminal domain of folliculin - a eukaryote- 106 specific protein which is known to be involved in membrane trafficking in humans13 (Figure 1c) in 107 Lokiarchaea. Furthermore, we retrieved conclusive hits for the ESP-related domains 108 Ezrin/radixin/moesin C-terminal domain and active zone protein ELKS in Lokiarchaeia. 109 110 A novel clade of rhodopsins: Recent findings reporting the presence of a novel family of rhodopsins14 111 (i.e. heliorhodopsins; abbreviated as HeR) in monoderms15 encouraged us to perform a dedicated 112 screening in all available Asgardaeota MAGs. The
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