The Epigenomic Landscape of Prokaryotes

ABSTRACT: DNA methylation is an important regulator of genome function in the eukaryotes, but it is currently unclear if the same is true in prokaryotes. While regulatory functions have been demonstrated for a small number of bacteria, there have been no large-scale studies of prokaryotic methylomes and the full repertoire of targets and biological functions of DNA methylation remains unclear. Here we applied single-molecule, real-time sequencing to directly study the methylomes of 232 phylogenetically diverse prokaryotes. Collectively, we identified 834 methylated motifs, enabling the specific annotation of 415 DNA methyltransferases (MTases), and adding substantially to existing databases of MTase specificities. While the majority of MTases function as components of restriction-modification systems, 139 MTases have no cognate restriction enzyme in the genome, suggesting some other functional role. Several of these ‘orphan’ MTases are conserved across species and exhibit patterns of DNA methylation consistent with known regulatory MTases. Based on these patterns of methylation, we identify candidate novel regulators of gene expression in several phyla of bacteria, and candidate regulators of DNA replication in Haloarchaea. Together these data substantially advance our knowledge of DNA restriction-modification systems, and hint at a wider role for methylation in prokaryotic genome regulation.

ORGANISM(S): Hydrogenovibrio crunogenus XCL-2 Pediococcus acidilactici AGR20 Desulfospira joergensenii DSM 10085 Chloroflexus aggregans DSM 9485 Lachnospiraceae bacterium AC2029 Treponema denticola ATCC 35405 Acetivibrio thermocellus DSM 1313 Clostridium algidicarnis Fervidobacterium nodosum Rt17-B1 Lacrimispora indolis SR3 Treponema succinifaciens DSM 2489 Limisalsivibrio acetivorans Escherichia coli CFT073 Clostridium sp. ASBs410 Holophaga foetida DSM 6591 Allomeiothermus silvanus DSM 9946 Clostridium sp. KNHs205 Methanothermus fervidus DSM 2088 Phaeobacter inhibens DSM 17395 Cellulophaga lytica DSM 7489 Butyrivibrio sp. AE3004 Lachnospiraceae bacterium AC2012 Butyrivibrio sp. AE3003 Bernardetia litoralis DSM 6794 Oceanicola sp. HL-35 Sphingomonas melonis C3 Asinibacterium sp. OR53 Staphylococcus epidermidis AG42 Methylophilus sp. 1 Kangiella aquimarina DSM 16071 Streptococcus equinus Saccharomonospora viridis DSM 43017 Rikenella microfusus DSM 15922 Methylophilus sp. 5 Sediminibacter sp. Hel_I_10 Prevotella sp. 10(H) Lachnoclostridium phytofermentans KNHs212 Gracilinema caldarium DSM 7334 Hippea alviniae EP5-r Salmonella enterica subsp. arizonae serovar 62:z4,z23:- Cellulomonas sp. KRMCY2 Thermoplasma volcanium GSS1 Mastigocladopsis repens PCC 10914 Sphaerobacter thermophilus DSM 20745 Pseudomonas aeruginosa NCAIM B.001380 Prevotella sp. HUN102 Methanocaldococcus jannaschii DSM 2661 Butyrivibrio sp. FCS014 Methanospirillum hungatei JF-1 Hydrogenovibrio sp. MA2-6 Methylotenera sp. 73s Methylophilus sp. 42 Thiobacillus denitrificans ATCC 25259 Lactiplantibacillus plantarum Dyadobacter fermentans DSM 18053 Methylophilaceae bacterium 11 Veillonella parvula DSM 2008 Halomicrobium katesii DSM 19301 Exiguobacterium acetylicum DSM 20416 Levilactobacillus brevis AG48 Haloterrigena turkmenica DSM 5511 Actinobacillus succinogenes 130Z Planctopirus limnophila DSM 3776 Agrobacterium fabrum str. C58 Streptosporangium roseum DSM 43021 Flavobacterium psychrophilum JIP02/86 Algoriphagus marincola HL-49 Methylobacterium sp. 10 Stutzerimonas stutzeri RCH2 Phocaeicola salanitronis DSM 18170 Thermanaerovibrio acidaminovorans DSM 6589 Syntrophobotulus glycolicus DSM 8271 Verrucomicrobia bacterium LP2A Gillisia sp. JM1 Cohnella panacarvi Gsoil 349 Pseudobutyrivibrio ruminis HUN009 Salmonella bongori NCTC 12419 Solitalea canadensis DSM 3403 Thiomonas sp. FB-6 Tolumonas lignilytica Hydrogenovibrio marinus DSM 11271 Caldicoprobacter oshimai DSM 21659 Methylobacter tundripaludum 21/22 Clostridioides mangenotii LM2 Streptobacillus moniliformis DSM 12112 Methanocorpusculum labreanum Z Thermogemmatispora carboxidivorans Thermobacillus composti KWC4 Ruminococcus albus AD2013 Streptomyces sp. WMMB 714 Desulfotignum balticum DSM 7044 Enterococcus faecalis 68A Marinithermus hydrothermalis DSM 14884 Peptostreptococcaceae bacterium VA2 Ruminococcus flavefaciens AE3010 Arthrobacter sp. 31Y Neisseria meningitidis FAM18 Exiguobacterium antarcticum DSM 14480 Ruminococcus sp. NK3A76 Methylorubrum extorquens AM1 Desulfobacca acetoxidans DSM 11109 Spirochaeta africana DSM 8902 Thermoanaerobacter sp. X514 Akkermansia muciniphila ATCC BAA-835 Solidesulfovibrio cf. magneticus IFRC170 Orenia marismortui DSM 5156 Xylella fastidiosa Temecula1 Selenomonas sp. AB3002 Acetobacterium woodii DSM 1030 Lactococcus lactis subsp. lactis Caldithrix abyssi DSM 13497 Calidithermus chliarophilus DSM 9957 Exiguobacterium aurantiacum DSM 6208 Nocardia sp. BMG51109 Persephonella Neisseria gonorrhoeae FA 1090 Flavimarina sp. Hel_I_48 Sinorhizobium medicae WSM1115 Echinicola vietnamensis DSM 17526 Staphylococcus aureus subsp. aureus USA300_TCH1516 Kallotenue papyrolyticum Rhodopseudomonas palustris CGA009 Maribacter sp. Hel_I_7 Acidobacteriaceae bacterium KBS 146 Sedimentitalea nanhaiensis DSM 24252 Anoxybacillus flavithermus WK1 Cellvibrionaceae bacterium 1162T.S.0a.05 Lachnoclostridium phytofermentans KNHs2132 Microbacterium sp. KROCY2 Robinsoniella sp. KNHs210 Parabacteroides distasonis ATCC 8503 Desulforegula conservatrix Mb1Pa Ruminiclostridium josui JCM 17888 Thermacetogenium phaeum DSM 12270 Pontibacter actiniarum DSM 19842 Teredinibacter purpureus Polaribacter sp. Hel_I_88 Enterococcus gallinarum Methylocystis sp. LW5 Methylobacterium sp. EUR3 AL-11 Palaeococcus ferrophilus DSM 13482 Alteromonas sp. ALT199 Niabella soli DSM 19437 Sulfurimonas denitrificans DSM 1251 Cellulophaga algicola DSM 14237 Flexistipes sinusarabici DSM 4947 Oxalobacteraceae bacterium AB_14 Zymomonas mobilis subsp. pomaceae ATCC 29192 Lachnobacterium bovis Hydrogenovibrio kuenenii DSM 12350 Bradyrhizobium elkanii USDA 76 Methylohalobius crimeensis 10Ki Meiothermus ruber DSM 1279 Alicyclobacillus macrosporangiidus CPP55 Methylotenera versatilis 79 Spirochaeta thermophila DSM 6578 Acetivibrio clariflavus 4-2a Teredinibacter turnerae Clostridium sp. 12(A) Aminiphilus circumscriptus DSM 16581 Salmonella enterica subsp. enterica serovar Paratyphi A str. ATCC 9150 Pseudarthrobacter chlorophenolicus A6 Xenorhabdus nematophila ATCC 19061 Thioalkalivibrio sp. ARh3 Escherichia coli str. K-12 substr. MG1655 Nitriliruptor alkaliphilus DSM 45188 Dinoroseobacter shibae DFL 12 = DSM 16493 Patulibacter minatonensis DSM 18081 Desulfohalovibrio reitneri Sebaldella termitidis ATCC 33386 Leptolyngbya sp. PCC 6406 Pelobacter seleniigenes DSM 18267 Methanohalophilus mahii DSM 5219 Selenomonas ruminantium AC2024 Actinosynnema mirum DSM 43827 Sporocytophaga myxococcoides DSM 11118 Desulfurobacterium sp. TC5-1 Pseudacidobacterium ailaaui Polaromonas sp. EUR3 1.2.1 Thiomicrospira pelophila DSM 1534 Gillisia limnaea DSM 15749 Ruminococcus sp. HUN007 Mediterraneibacter gnavus AGR2154 Exiguobacterium oxidotolerans JCM 12280 Thermosipho melanesiensis BI429 Pseudofrankia sp. DC12 Pedobacter heparinus DSM 2366 Acetivibrio thermocellus ATCC 27405 Psychrilyobacter atlanticus DSM 19335 Sulfolobus acidocaldarius DSM 639 Nitratifractor salsuginis DSM 16511 Hippea sp. KM1 Bryobacter aggregatus MPL3 Exiguobacterium chiriqhucha Aminobacterium colombiense DSM 12261 Mycoplasmopsis bovis PG45 Acidobacteriaceae bacterium TAA 166 Acidovorax sp. JHL-3 Geopsychrobacter electrodiphilus DSM 16401 Polycyclovorans algicola TG408 Bifidobacterium longum subsp. infantis ATCC 15697 = JCM 1222 = DSM 20088 Ruminococcaceae bacterium AE2021 Clostridium perfringens ATCC 13124 Klebsiella aerogenes FGI35 Eubacterium sp. AB3007 Sulfurospirillum barnesii SES-3 Klebsiella oxytoca BRL6-2 Bacteroides sp. 14(A) Salmonella enterica subsp. enterica serovar Paratyphi B str. SPB7 Syntrophothermus lipocalidus DSM 12680 Coraliomargarita akajimensis DSM 45221 Hirschia baltica ATCC 49814 Sediminispirochaeta smaragdinae DSM 11293 Clostridioides difficile 630 Galbibacter orientalis Shewanella woodyi ATCC 51908 Staphylothermus marinus F1 Rhizobium etli CIAT 652 Xanthobacter sp. 91 Nocardia sp. BMG111209 Lachnospiraceae bacterium AC2031 Thermoplasma acidophilum DSM 1728 Capnocytophaga ochracea DSM 7271 Lacrimispora indolis DSM 755 Corynebacterium aurimucosum ATCC 700975 Pyrococcus horikoshii OT3 Cronobacter Bacillus spizizenii str. W23

PROVIDER: GSE69872 | GEO | 2016/01/20

SECONDARY ACCESSION(S): PRJNA287040

REPOSITORIES: GEO