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Comprehensive Evolutionary Analysis of Re- Verse Report for Taikichiro Mori Memorial Research Grants 2019 (2019 年度森基金研究成果報告書) 生命の複製に関わる酵素の新規発見と機能解明 Comprehensive evolutionary analysis of re- verse transcriptases in viruses and prokary- otes Shohei Nagata Institute for Advanced Biosciences, Keio University, Tsuruoka 997-0035, Japan and Sys- tems Biology Program, Graduate School of Media and Governance, Keio University, Fu- jisawa 252-0882, Japan. Abstract Reverse transcriptases (RTs) are enzymes that polymerize DNA from RNA tem- plates. RTs are usually thought to be viral and eukaryotic elements, but they are also present in bacteria. Bacterial RTs are seemed to be ancestors of eukaryotic RTs and several types are identified i.e. group II introns, retrons, CRISPR/Cas- associated RTs, diversity-generating retroelements (DGRs), and Abi -like genes. Recently, several studies reported that the existence of RTs in a recently reported bacterial group, candidate phyla radiation (CPR). These CPR RTs are thought to have an important role and functions in CPR bacterial ecologies since they retain RT genes while lacking numerous biosynthetic pathways. In this study, I compre- hensively collected RT-like sequences from CPR genomes and systematically char- acterized RT functions and evolution. Using known functional domain profiles in RTs as queries, sequence similarity search was performed against 804 near-complete genomes of CPR bacteria in the database. I obtained 514 RT sequences and these RTs are widely distributed in CPR phyla. It is known that CPR bacteria utilize RTs involved in DGRs to adapt rapidly changing environments, I found RTs related to group II introns, retrons, and abortive infection (Abi). I will discuss possible roles and evolution of RTs in CPR bacteria. Contact: [email protected] otes thereafter. In addition to viruses infecting eu- 1 Introduction karyotic organisms (retrovirus, pararetrovirus, Central dogma in molecular biology is a flow of in- hepadnavirus), the existence of a RT homologous formation that genetic information retained on DNA region in long terminal repeat (LTR) retroelement, is transcribed into mRNA and translated into protein, non-LTR retroelement, telomerase has been re- which was proposed in 1958. However, in 1970, an vealed. RNA-dependent DNA polymerase (reverse tran- In 1989, retron, one of the reverse transcriptase scriptase; RT), which synthesizes DNA based on (RT) was found in bacteria [3,4]. Even after that, RNA, reversed this flow [1,2]. This was discovered various types of RTs were discovered in bacteria by studies of tumor-associated retroviruses that in- and archaea by the discovery of group II intron [5– fect eukaryotes, and various types of RT enzymes 7] and diversity-generating retroelements (DGRs) have been discovered primarily related to eukary- [8–10] etc. Retrons consist of an RT and an adjacent repeat sequence but its function remains unknown. 1 S.Nagata Group II introns are retroelements consists of cata- of diversification are not well understood. In this lytic RNA and an RT protein which mediate splic- study, a comprehensive analysis was performed on ing and mobility reactions [11–13]. DGRs are retro- the RT sequence from CPR bacterial genomes, to elements that lost mobility functions and use reverse revealLETTERS roles and evolutionNATURE of MICROBIOLOGYRTs in CPRDOI: 10.1038/NMICROBIOL.2016.48 bacteria. transcription to generate sequence variations in spe- (Tenericutes) Bacteria Actinobacteria Armatimonadetes Nomurabacteria Kaiserbacteria cific target genes [10]. Then, it was revealed that RT Zixibacteria Atribacteria Adlerbacteria Cloacimonetes Aquificae Chloroflexi Campbellbacteria Fibrobacteres Calescamantes Gemmatimonadetes Caldiserica Firmicutes WOR-3 Dictyoglomi Cyanobacteria is a gene that is widely present in the three domains TA06 Thermotogae Poribacteria Deinococcus-Therm. Latescibacteria Synergistetes Giovannonibacteria BRC1 Fusobacteria Melainabacteria Wolfebacteria Marinimicrobia Jorgensenbacteria of life (bacteria, archaea, eukaryotes) and viruses RBX1 Ignavibacteria Bacteroidetes WOR1 Chlorobi Caldithrix Azambacteria [14–17]. In bacteria, it is also known that RT ho- PVC Parcubacteria superphylum Yanofskybacteria Planctomycetes Moranbacteria Elusimicrobia Chlamydiae, mologous region exists also in abi gene related to Lentisphaerae, Magasanikbacteria Verrucomicrobia Uhrbacteria Falkowbacteria Candidate Omnitrophica Phyla Radiation abortive infection (Abi) to phage [18,19] and cas1 SM2F11 Rokubacteria NC10 Aminicentantes Peregrinibacteria Acidobacteria Tectomicrobia, Modulibacteria Gracilibacteria BD1-5, GN02 Nitrospinae Absconditabacteria SR1 Nitrospirae Saccharibacteria gene of CRISPR/Cas immune system [20,21]. Dadabacteria Berkelbacteria Deltaprotebacteria (Thermodesulfobacteria) Chrysiogenetes Deferribacteres Three bacterial RT-related proteins are involved in Hydrogenedentes NKB19 Woesebacteria Spirochaetes Shapirobacteria Wirthbacteria Amesbacteria TM6 Collierbacteria Epsilonproteobacteria Pacebacteria phage resistance; AbiA, AbiK, and Abi-P2 [15]. Beckwithbacteria Roizmanbacteria Dojkabacteria WS6 Gottesmanbacteria CPR1 Levybacteria CPR3 Daviesbacteria Microgenomates AbiA and AbiK are thought to provide phage im- Katanobacteria Curtissbacteria Alphaproteobacteria WWE3 Zetaproteo. munity through abortive infection. Also, recently Acidithiobacillia Betaproteobacteria Major lineages with isolated representative: italics Major lineage lacking isolated representative: there have been reports that many uncharacterized 0.4 Gammaproteobacteria RT-like sequences mainly exist in bacteria [15,20,21]. However, what kind of functions/activi- ties they possess, and how they divergences were Micrarchaeota Diapherotrites Eukaryotes Nanohaloarchaeota Aenigmarchaeota Loki. unclear. Parvarchaeota Thor. Korarch. DPANN Crenarch. More recently, it has become clear that a vast un- Pacearchaeota Bathyarc. Nanoarchaeota YNPFFA Woesearchaeota Aigarch. Opisthokonta Altiarchaeales Halobacteria Z7ME43 known microbial strain group exists in bacteria by Methanopyri TACK Methanococci Excavata Archaea Hadesarchaea Thermococci Thaumarchaeota Archaeplastida Methanobacteria technological advances in metagenomic analysis Thermoplasmata Chromalveolata Archaeoglobi Methanomicrobia Amoebozoa and single-cell genomics. Metagenomic approach Figure 1 | A current view of the tree of life, encompassing the total diversity represented by sequenced genomes. The tree includes 92 named bacterial Figurephyla, 26 archaeal phyla1. and1 allAfive ofcurrent the Eukaryotic supergroups. view Major lineages of are assignedthe arbitrary tree colours andof named, life. with well-characterized The phy- lineage revealed huge diversity of previously unknown names, in italics. Lineages lacking an isolated representative are highlighted with non-italicized names and red dots. For details on taxon sampling and tree inference, see Methods. The names Tenericutes and Thermodesulfobacteria are bracketed to indicate that these lineages branch within the Firmicutesand logeneticthe Deltaproteobacteria, respectively.tree Eukaryotic of supergroupsbacteria, are noted, but notarchaea, otherwise delineated dueand to the low resolutioneukaryotes, of these lineages. The CPR in- phyla of bacteria and archaea since they have differ- phyla are assigned a single colour as they are composed entirely of organisms without isolated representatives, and are still in the process of definition at cludlower taxonomicing levels. 92 The completenamed ribosomal protein bacterial tree is available in rectangular phyla, format with 26 full bootstrap archaeal values as Supplementary phyla Fig. 1 andin and ent forms of 16S rRNA sequences. In bacteria, these Newick format in Supplementary Dataset 2. all2 five of the Eukaryotic supergroupsNATURE. MICROBIOLOGY The tree| www.nature.com/naturemicrobiology was esti- metagenomically recovered bacterial strain was de- mated by maximum© 2016-likelihood Macmillan Publishers Limited. All method rights reserved using concatena- scribed as candidate phyla radiation (CPR) and tion of ribosomal protein sequences. The figure adapted comprises at least 15% of all bacteria [22]. The CPR from reference [23]. seems to be monophyletic and clearly separated from other bacteria (Figure 1.1; Castelle and Banfield, 2018; Hug et al., 2016). CPR bacteria are 2 Methods widely distributed across the various environments such as human microbiome [25] , deep subsurface 2.1 Data sources sediments [26], the dolphin mouth [27], drinking Complete genome sequences of bacteria and ar- water [28], soil [29], marine sediment [30] and other chaea were downloaded from the Reference Se- environments [24,31]. quence Database (RefSeq) [32] at the National Cen- CPR bacteria have various unusual features com- ter for Biotechnology Information (NCBI) as of pared to non-CPR bacteria. CPR genomes are less May 2018. The acquired genomes (denoted as Ref- than 1.5Mb while the genome size of non-CPR bac- Seq prokaryotes in this manuscript) were 9,078 ge- teria, Escherichia coli, is 4.6Mb. Most of them lost nomes (total of bacteria 8,825, archaea 253, respec- TCA-cycle genes and they have intron regions in tively). rRNA genes [22,31]. It is sometimes questioned Nearly full-length (restored by ≥ 70% based on whether CPR bacteria is a cellular organism, at least, the estimated full length) of 804 genomes (790 spe- CPR genomes encode genetic systems for cell divi- cies) of CPR bacteria were obtained from NCBI sion (e.g. Fts-Z-based mechanisms, not found in GenBank based on Hug et al. [23]. some symbionts
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