[en] Prochlorococcus, a cyanobacteria genus of the smallest and most abundant oceanic phototrophs, encompasses ecotype strains adapted to high-light (HL) and low-light (LL) niches. To elucidate the adaptive evolution of this genus, we analyzed 40 Prochlorococcus marinus ORFeomes, including two cornerstone strains, MED4 and NATL1A. Employing deep learning with robust statistical methods, we detected new protein family distributions in the strains and identified key genes differentiating the HL and LL strains. The HL strains harbor genes (ABC-2 transporters) related to stress resistance, such as DNA repair and RNA processing, while the LL strains exhibit unique chlorophyll adaptations (ion transport proteins, HEAT repeats). Additionally, we report the finding of variable, depth-dependent endogenous viral elements in the 40 strains. To generate biological resources to experimentally study the HL and LL adaptations, we constructed the ORFeomes of two representative strains, MED4 and NATL1A synthetically, covering 99% of the annotated protein-coding sequences of the two species, totaling 3976 cloned, sequence-verified open reading frames (ORFs). These comparative genomic analyses, paired with MED4 and NATL1A ORFeomes, will facilitate future genotype-to-phenotype mappings and the systems biology exploration of Prochlorococcus ecology.
Disciplines :
Biotechnology
Author, co-author :
Daakour, Sarah ; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates
Nelson, David R ; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates
Fu, Weiqi ; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Department of Marine Science, Ocean College, Zhejiang University, Zhoushan 316021, China
Jaiswal, Ashish ; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates
Dohai, Bushra; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Helmholtz Center Munich, Institute of Network Biology (INET), German Research Center for Environmental Health, 85764 Munich, Germany
Alzahmi, Amnah Salem; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Laboratory of Viral Interactomes Networks, Unit of Molecular & Computational Biology, Interdisciplinary Cluster for Applied Genoproteomics (GIGA Institute), University of Liège, 4000 Liège, Belgium
Koussa, Joseph; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Department of Biology, New York University, New York, NY 10012, USA ; Department of Chemical and Biological Sciences, Montgomery College, Germantown, MD 20850, USA
Huang, Xiaoluo; Genome Synthesis and Editing Platform, China National GeneBank (CNGB), BGI-Research, Shenzhen 518120, China ; Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Beijing 100045, China
Shen, Yue; Genome Synthesis and Editing Platform, China National GeneBank (CNGB), BGI-Research, Shenzhen 518120, China
Twizere, Jean-Claude ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases - Viral Interactomes Network ; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates
Salehi-Ashtiani, Kourosh ; Center for Genomics and Systems Biology (CGSB), New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates ; Division of Science and Math, New York University-Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates
Language :
English
Title :
Adaptive Evolution Signatures in Prochlorococcus: Open Reading Frame (ORF)eome Resources and Insights from Comparative Genomics.
Publication date :
20 August 2024
Journal title :
Microorganisms
eISSN :
2076-2607
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
NYUAD Faculty Research Funds NYU Abu Dhabi Research Institute
Funding text :
This research was supported by NYUAD Faculty Research Funds (AD060) and Tamkeen under the NYU Abu Dhabi Research Institute Award to the NYUAD Center for Genomics and Systems Biology (73 71210 CGSB9). J.-C.T. is a \u201CMa\u00EEtre de Recherche\u201D of the Fonds National de la recherche Scientifique (FRS-FNRS, Belgium).
Percival S.L. Williams D.W. Microbiology of Waterborne Diseases 2nd ed. Percival S.L. Yates M.V. Williams D.W. Chalmers R.M. Gray N.F. Academic Press London, UK 2014 79 88
Demoulin C.F. Lara Y.J. Cornet L. François C. Baurain D. Wilmotte A. Javaux E.J. Cyanobacteria evolution: Insight from the fossil record Free Radic. Biol. Med. 2019 140 206 223 10.1016/j.freeradbiomed.2019.05.007 31078731
Ruffing A.M. Engineered cyanobacteria: Teaching an old bug new tricks Bioeng. Bugs 2011 2 136 149 10.4161/bbug.2.3.15285 21637004
Goericke R. Welschmeyer N.A. The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea Deep Sea Res. Part I Oceanogr. Res. Pap. 1993 40 2283 2294 10.1016/0967-0637(93)90104-B
Scanlan D.J. Ostrowski M. Mazard S. Dufresne A. Garczarek L. Hess W.R. Post A.F. Hagemann M. Paulsen I. Partensky F. Ecological genomics of marine picocyanobacteria Microbiol. Mol. Biol. Rev. 2009 73 249 299 10.1128/MMBR.00035-08 19487728
Partensky F. Hess W.R. Vaulot D. Prochlorococcus, a marine photosynthetic prokaryote of global significance Microbiol. Mol. Biol. Rev. 1999 63 106 10.1128/MMBR.63.1.106-127.1999 10066832
Moore L.R. Rocap G. Chisholm S.W. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes Nature 1998 393 464 467 10.1038/30965 9624000
Luo H. Huang Y. Stepanauskas R. Tang J. Excess of non-conservative amino acid changes in marine bacterioplankton lineages with reduced genomes Nat. Microbiol. 2017 2 17091 10.1038/nmicrobiol.2017.91 28604700
Kettler G.C. Martiny A.C. Huang K. Zucker J. Coleman M.L. Rodrigue S. Chen F. Lapidus A. Ferriera S. Johnson J. et al. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus PLoS Genet. 2007 3 e231 10.1371/journal.pgen.0030231 18159947
O’Leary N.A. Wright M.W. Brister J.R. Ciufo S. Haddad D. McVeigh R. Rajput B. Robbertse B. Smith-White B. Ako-Adjei D. et al. Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation Nucleic Acids Res. 2015 44 D733 D745 10.1093/nar/gkv1189 26553804
Dufresne A. Salanoubat M. Partensky F. Artiguenave F. Axmann I.M. Barbe V. Duprat S. Galperin M.Y. Koonin E.V. Le Gall F. et al. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome Proc. Natl. Acad. Sci. USA 2003 100 10020 10025 10.1073/pnas.1733211100 12917486
Moore L.R. Goericke R. Chisholm S.W. Comparative physiology of Synechococcus and Prochlorococcus: Influence of light and temperature on growth, pigments, fluorescence and absorptive properties Mar. Ecol. Prog. Ser. 1995 116 259 275 10.3354/meps116259
Rocap G. Larimer F.W. Lamerdin J. Malfatti S. Chain P. Ahlgren N.A. Arellano A. Coleman M. Hauser L. Hess W.R. et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation Nature 2003 424 1042 1047 10.1038/nature01947
Metsalu T. Vilo J. ClustVis: A web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap Nucleic Acids Res. 2015 43 W566 W570 10.1093/nar/gkv468 25969447
Rual J.-F. Hirozane-Kishikawa T. Hao T. Bertin N. Li S. Dricot A. Li N. Rosenberg J. Lamesch P. Vidalain P.-O. et al. Human ORFeome Version 1.1: A Platform for Reverse Proteomics Genome Res. 2004 14 2128 2135 10.1101/gr.2973604 15489335
Darzi Y. Letunic I. Bork P. Yamada T. iPath3.0: Interactive pathways explorer v3 Nucleic Acids Res. 2018 46 W510 W513 10.1093/nar/gky299
Conesa A. Götz S. García-Gómez J.M. Terol J. Talón M. Robles M. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research Bioinformatics 2005 21 3674 3676 10.1093/bioinformatics/bti610
Rual J.-F. Venkatesan K. Hao T. Hirozane-Kishikawa T. Dricot A. Li N. Berriz G.F. Gibbons F.D. Dreze M. Ayivi-Guedehoussou N. et al. Towards a proteome-scale map of the human protein–protein interaction network Nature 2005 437 1173 1178 10.1038/nature04209
Weitz J.S. Wilhelm S.W. Ocean viruses and their effects on microbial communities and biogeochemical cycles F1000 Biol. Rep. 2012 4 17 10.3410/B4-17
Chen M.-Y. Teng W.-K. Zhao L. Hu C.-X. Zhou Y.-K. Han B.-P. Song L.-R. Shu W.-S. Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation ISME J. 2021 15 211 227 10.1038/s41396-020-00775-z
Yang F. Miao Y. Liu Y. Botella J.R. Li W. Li K. Song C.-P. Function of Protein Kinases in Leaf Senescence of Plants Front. Plant Sci. 2022 13 864215 10.3389/fpls.2022.864215 35548290
Andrés G. María F.F. María-Teresa B. María-Luisa P. Emma S. Cyanobacteria Archana T. IntechOpen Rijeka, Croatia 2018 Chapter 6
Jia A. Zheng Y. Chen H. Wang Q. Regulation and Functional Complexity of the Chlorophyll-Binding Protein IsiA Front. Microbiol. 2021 12 774107 10.3389/fmicb.2021.774107 34867913
Kroh G.E. Pilon M. Regulation of iron homeostasis and use in chloroplasts Int. J. Mol. Sci. 2020 21 3395 10.3390/ijms21093395
Christensen Q.H. Cronan J.E. Lipoic acid synthesis: A new family of octanoyltransferases generally annotated as lipoate protein ligases Biochemistry 2010 49 10024 10036 10.1021/bi101215f
Cronan J.E. Assembly of Lipoic Acid on Its Cognate Enzymes: An Extraordinary and Essential Biosynthetic Pathway Microbiol. Mol. Biol. Rev. 2016 80 429 450 10.1128/MMBR.00073-15
Bristow L.A. Mohr W. Ahmerkamp S. Kuypers M.M.M. Nutrients that limit growth in the ocean Curr. Biol. 2017 27 R474 R478 10.1016/j.cub.2017.03.030 28586682
Latifi A. Ruiz M. Zhang C.-C. Oxidative stress in cyanobacteria FEMS Microbiol. Rev. 2009 33 258 278 10.1111/j.1574-6976.2008.00134.x
Santamaría-Gómez J. Ochoa de Alda J.A.G. Olmedo-Verd E. Bru-Martínez R. Luque I. Sub-Cellular Localization and Complex Formation by Aminoacyl-tRNA Synthetases in Cyanobacteria: Evidence for Interaction of Membrane-Anchored ValRS with ATP Synthase Front. Microbiol. 2016 7 857 10.3389/fmicb.2016.00857
Luque I. Riera-Alberola M.L. Andújar A. Ochoa de Alda J.A.G. Intraphylum Diversity and Complex Evolution of Cyanobacterial Aminoacyl-tRNA Synthetases Mol. Biol. Evol. 2008 25 2369 2389 10.1093/molbev/msn197 18775898
Song K. Baumgartner D. Hagemann M. Muro-Pastor A.M. Maaß S. Becher D. Hess W.R. AtpΘ is an inhibitor of F0F1 ATP synthase to arrest ATP hydrolysis during low-energy conditions in cyanobacteria Curr. Biol. 2022 32 136 148.e135 10.1016/j.cub.2021.10.051
Cassier-Chauvat C. Veaudor T. Chauvat F. Comparative Genomics of DNA Recombination and Repair in Cyanobacteria: Biotechnological Implications Front. Microbiol. 2016 7 1809 10.3389/fmicb.2016.01809 27881980
Kolowrat C. Partensky F. Mella-Flores D. Le Corguillé G. Boutte C. Blot N. Ratin M. Ferréol M. Lecomte X. Gourvil P. et al. Ultraviolet stress delays chromosome replication in light/dark synchronized cells of the marine cyanobacterium Prochlorococcus marinus PCC9511 BMC Microbiol. 2010 10 204 10.1186/1471-2180-10-204 20670397
Osburne M.S. Holmbeck B.M. Frias-Lopez J. Steen R. Huang K. Kelly L. Coe A. Waraska K. Gagne A. Chisholm S.W. UV hyper-resistance in Prochlorococcus MED4 results from a single base pair deletion just upstream of an operon encoding nudix hydrolase and photolyase Environ. Microbiol. 2010 12 1978 1988 10.1111/j.1462-2920.2010.02203.x 20345942
Cassier-Chauvat C. Chauvat F. Responses to oxidative and heavy metal stresses in cyanobacteria: Recent advances Int. J. Mol. Sci. 2014 16 871 886 10.3390/ijms16010871 25561236
Berube P.M. Rasmussen A. Braakman R. Stepanauskas R. Chisholm S.W. Emergence of trait variability through the lens of nitrogen assimilation in Prochlorococcus eLife 2019 8 e41043 10.7554/eLife.41043
Varkey D. Mazard S. Ostrowski M. Tetu S.G. Haynes P. Paulsen I.T. Effects of low temperature on tropical and temperate isolates of marine Synechococcus ISME J. 2016 10 1252 1263 10.1038/ismej.2015.179
Knoll A. Puchta H. The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants J. Exp. Bot. 2010 62 1565 1579 10.1093/jxb/erq357 21081662
Hilbert M. Karow A.R. Klostermeier D. The mechanism of ATP-dependent RNA unwinding by DEAD box proteins Biol. Chem. 2009 390 1237 1250 10.1515/BC.2009.135
Muzzopappa F. Wilson A. Yogarajah V. Cot S. Perreau F. Montigny C. De Carbon C.B. Kirilovsky D. Paralogs of the C-Terminal Domain of the Cyanobacterial Orange Carotenoid Protein Are Carotenoid Donors to Helical Carotenoid Proteins Plant Physiol. 2017 175 1283 1303 10.1104/pp.17.01040 28935842
Cerveny L. Straskova A. Dankova V. Hartlova A. Ceckova M. Staud F. Stulik J. Tetratricopeptide repeat motifs in the world of bacterial pathogens: Role in virulence mechanisms Infect. Immun. 2013 81 629 635 10.1128/IAI.01035-12 23264049
Grove T.Z. Cortajarena A.L. Regan L. Ligand binding by repeat proteins: Natural and designed Curr. Opin. Struct. Biol. 2008 18 507 515 10.1016/j.sbi.2008.05.008 18602006
Rast A. Rengstl B. Heinz S. Klingl A. Nickelsen J. The Role of Slr0151, a Tetratricopeptide Repeat Protein from Synechocystis sp. PCC 6803, during Photosystem II Assembly and Repair Front. Plant Sci. 2016 7 605 10.3389/fpls.2016.00605 27200072
Biller S.J. Coe A. Chisholm S.W. Torn apart and reunited: Impact of a heterotroph on the transcriptome of Prochlorococcus ISME J. 2016 10 2831 2843 10.1038/ismej.2016.82 27258949
Kong R. Xu X. Hu Z. A TPR-family membrane protein gene is required for light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. PCC 6803 FEMS Microbiol. Lett. 2003 219 75 79 10.1016/S0378-1097(02)01205-3 12594026
Morimoto K. Nishio K. Nakai M. Identification of a novel prokaryotic HEAT-repeats-containing protein which interacts with a cyanobacterial IscA homolog FEBS Lett. 2002 519 123 127 10.1016/S0014-5793(02)02736-9 12023030
Mella-Flores D. Six C. Ratin M. Partensky F. Boutte C. Le Corguillé G. Marie D. Blot N. Gourvil P. Kolowrat C. et al. Prochlorococcus and Synechococcus have Evolved Different Adaptive Mechanisms to Cope with Light and UV Stress Front. Microbiol. 2012 3 285 10.3389/fmicb.2012.00285 23024637
Ofaim S. Sulheim S. Almaas E. Sher D. Segrè D. Dynamic Allocation of Carbon Storage and Nutrient-Dependent Exudation in a Revised Genome-Scale Model of Prochlorococcus Front. Genet. 2021 12 586293 10.3389/fgene.2021.586293 33633777
Bibby T.S. Mary I. Nield J. Partensky F. Barber J. Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem Nature 2003 424 1051 1054 10.1038/nature01933 12944966
Gisriel C.J. Shen G. Flesher D.A. Kurashov V. Golbeck J.H. Brudvig G.W. Amin M. Bryant D.A. Structure of a dimeric photosystem II complex from a cyanobacterium acclimated to far-red light J. Biol. Chem. 2023 299 102815 10.1016/j.jbc.2022.102815 36549647
Safferman R. Cannon R. Desjardins P. Gromov B. Haselkorn R. Sherman L. Shilo M. Classification and nomenclature of viruses of cyanobacteria Intervirology 1983 19 61 66 10.1159/000149339 6408019
Dammeyer T. Bagby S.C. Sullivan M.B. Chisholm S.W. Frankenberg-Dinkel N. Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria Curr. Biol. 2008 18 442 448 10.1016/j.cub.2008.02.067 18356052
Voorhies A.A. Eisenlord S.D. Marcus D.N. Duhaime M.B. Biddanda B.A. Cavalcoli J.D. Dick G.J. Ecological and genetic interactions between cyanobacteria and viruses in a low-oxygen mat community inferred through metagenomics and metatranscriptomics Environ. Microbiol. 2016 18 358 371 10.1111/1462-2920.12756
Moniruzzaman M. Weinheimer A.R. Martinez-Gutierrez C.A. Aylward F.O. Widespread endogenization of giant viruses shapes genomes of green algae Nature 2020 588 141 145 10.1038/s41586-020-2924-2
Rozenberg A. Oppermann J. Wietek J. Lahore R.G.F. Sandaa R.-A. Bratbak G. Hegemann P. Béjà O. Lateral Gene Transfer of Anion-Conducting Channelrhodopsins between Green Algae and Giant Viruses Curr. Biol. 2020 30 4910 4920.e4915 10.1016/j.cub.2020.09.056
Chelkha N. Levasseur A. La Scola B. Colson P. Host-virus interactions and defense mechanisms for giant viruses Ann. N. Y. Acad. Sci. 2021 1486 39 57 10.1111/nyas.14469
Yoosuf N. Pagnier I. Fournous G. Robert C. La Scola B. Raoult D. Colson P. Complete genome sequence of Courdo11 virus, a member of the family Mimiviridae Virus Genes 2014 48 218 223 10.1007/s11262-013-1016-x
de Aquino I.L.M. Serafim M.S.M. Machado T.B. Azevedo B.L. Cunha D.E.S. Ullmann L.S. Araújo J.P. Jr. Abrahão J.S. Diversity of Surface Fibril Patterns in Mimivirus Isolates J. Virol. 2023 97 e0182422 10.1128/jvi.01824-22 36728417
Bisio H. Legendre M. Giry C. Philippe N. Alempic J.-M. Jeudy S. Abergel C. Evolution of giant pandoravirus revealed by CRISPR/Cas9 Nat. Commun. 2023 14 428 10.1038/s41467-023-36145-4 36702819
Hikida H. Okazaki Y. Zhang R. Nguyen T.T. Ogata H. A rapid genome-wide analysis of isolated giant viruses using MinION sequencing Environ. Microbiol. 2023 25 2621 2635 10.1111/1462-2920.16476 37543720
Esmael A. Agarkova I.V. Dunigan D.D. Zhou Y. Van Etten J.L. Viral DNA Accumulation Regulates Replication Efficiency of Chlorovirus OSy-NE5 in Two Closely Related Chlorella variabilis Strains Viruses 2023 15 1341 10.3390/v15061341
Fernández-García J.L. de Ory A. Brussaard C.P.D. de Vega M. Phaeocystis globosa Virus DNA Polymerase X: A “Swiss Army knife”, Multifunctional DNA polymerase-lyase-ligase for Base Excision Repair Sci. Rep. 2017 7 6907 10.1038/s41598-017-07378-3
Derelle E. Monier A. Cooke R. Worden A.Z. Grimsley N.H. Moreau H. Diversity of Viruses Infecting the Green Microalga Ostreococcus lucimarinus J. Virol. 2015 89 5812 5821 10.1128/JVI.00246-15
Delaroque N. Maier I. Knippers R. Müller D.G. Persistent virus integration into the genome of its algal host, Ectocarpus siliculosus (Phaeophyceae) J. Gen. Virol. 1999 80 Pt 6 1367 1370 10.1099/0022-1317-80-6-1367 10374952
Haller S.L. Peng C. McFadden G. Rothenburg S. Poxviruses and the evolution of host range and virulence Infect. Genet. Evol. 2014 21 15 40 10.1016/j.meegid.2013.10.014
Kehr J.C. Dittmann E. Biosynthesis and function of extracellular glycans in cyanobacteria Life 2015 5 164 180 10.3390/life5010164
Walhout A.J. Temple G. Brasch M. Hartley J. Lorson M. Van Den Heuvel S. Vidal M. GATEWAY recombinational cloning: Application to the cloning of large numbers of open reading frames or ORFeomes Methods in Enzymology Elsevier Amsterdam, The Netherlands 2000 Volume 328 575 592 IN7
Hartley J.L. Temple G.F. Brasch M.A. DNA cloning using in vitro site-specific recombination Genome Res. 2000 10 1788 1795 10.1101/gr.143000 11076863
Dreze M. Monachello D. Lurin C. Cusick M.E. Hill D.E. Vidal M. Braun P. High-Quality Binary Interactome Mapping Methods in Enzymology Academic Press New York, NY, USA 2010 Volume 470 281 315
Sánchez-Baracaldo P. Origin of marine planktonic cyanobacteria Sci. Rep. 2015 5 17418 10.1038/srep17418
Ulloa O. Henríquez-Castillo C. Ramírez-Flandes S. Plominsky A.M. Murillo A.A. Morgan-Lang C. Hallam S.J. Stepanauskas R. The cyanobacterium Prochlorococcus has divergent light-harvesting antennae and may have evolved in a low-oxygen ocean Proc. Natl. Acad. Sci. USA 2021 118 e2025638118 10.1073/pnas.2025638118 33707213
El-Seedi H.R. El-Mallah M.F. Yosri N. Alajlani M. Zhao C. Mehmood M.A. Du M. Ullah H. Daglia M. Guo Z. et al. Review of Marine Cyanobacteria and the Aspects Related to Their Roles: Chemical, Biological Properties, Nitrogen Fixation and Climate Change Mar. Drugs 2023 21 439 10.3390/md21080439
Flombaum P. Gallegos J.L. Gordillo R.A. Rincón J. Zabala L.L. Jiao N. Karl D.M. Li W.K. Lomas M.W. Veneziano D. et al. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus Proc. Natl. Acad. Sci. USA 2013 110 9824 9829 10.1073/pnas.1307701110
Puxty R.J. Millard A.D. Evans D.J. Scanlan D.J. Shedding new light on viral photosynthesis Photosynth. Res. 2015 126 71 97 10.1007/s11120-014-0057-x
James J.E. Nelson P.G. Masel J. Differential Retention of Pfam Domains Contributes to Long-term Evolutionary Trends Mol. Biol. Evol. 2023 40 msad073 10.1093/molbev/msad073 36947137
Godbold J.A. Calosi P. Ocean acidification and climate change: Advances in ecology and evolution Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013 368 20120448 10.1098/rstb.2012.0448 23980247
Beardall J. Stojkovic S. Larsen S. Living in a high CO2 world: Impacts of global climate change on marine phytoplankton Plant Ecol. Divers. 2009 2 191 205 10.1080/17550870903271363
Hallegraeff G.M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge 1 J. Phycol. 2010 46 220 235 10.1111/j.1529-8817.2010.00815.x
Shestakov S.V. Karbysheva E.A. The role of viruses in the evolution of cyanobacteria Biol. Bull. Rev. 2015 5 527 537 10.1134/S2079086415060079
Zhaxybayeva O. Doolittle W.F. Papke R.T. Gogarten J.P. Intertwined evolutionary histories of marine Synechococcus and Prochlorococcus marinus Genome Biol. Evol. 2009 1 325 339 10.1093/gbe/evp032 20333202
Zeidner G. Bielawski J.P. Shmoish M. Scanlan D.J. Sabehi G. Béjà O. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates Environ. Microbiol. 2005 7 1505 1513 10.1111/j.1462-2920.2005.00833.x 16156724
Lindell D. Jaffe J.D. Coleman M.L. Futschik M.E. Axmann I.M. Rector T. Kettler G. Sullivan M.B. Steen R. Hess W.R. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution Nature 2007 449 83 86 10.1038/nature06130 17805294
Gong W. Shen Y.-P. Ma L.-G. Pan Y. Du Y.-L. Wang D.-H. Yang J.-Y. Hu L.-D. Liu X.-F. Dong C.-X. et al. Genome-wide ORFeome cloning and analysis of Arabidopsis transcription factor genes Plant Physiol. 2004 135 773 782 10.1104/pp.104.042176 15208423
Kang S.E. Breton G. Pruneda-Paz J.L. Construction of Arabidopsis Transcription Factor ORFeome Collections and Identification of Protein-DNA Interactions by High-Throughput Yeast One-Hybrid Screens Methods Mol. Biol. 2018 1794 151 182
Lamesch P. Li N. Milstein S. Fan C. Hao T. Szabo G. Hu Z. Venkatesan K. Bethel G. Martin P. et al. hORFeome v3.1: A resource of human open reading frames representing over 10,000 human genes Genomics 2007 89 307 315 10.1016/j.ygeno.2006.11.012 17207965
Rual J.-F. Hill D.E. Vidal M. ORFeome projects: Gateway between genomics and omics Curr. Opin. Chem. Biol. 2004 8 20 25 10.1016/j.cbpa.2003.12.002
Rajagopala S.V. Yamamoto N. Zweifel A.E. Nakamichi T. Huang H.-K. Mendez-Rios J.D. Franca-Koh J. Boorgula M.P. Fujita K. Suzuki K.-I. et al. The Escherichia coli K-12 ORFeome: A resource for comparative molecular microbiology BMC Genom. 2010 11 470 10.1186/1471-2164-11-470 20701780
Özkan E. Carrillo R.A. Eastman C.L. Weiszmann R. Waghray D. Johnson K.G. Zinn K. Celniker S.E. Garcia K.C. An extracellular interactome of immunoglobulin and LRR proteins reveals receptor-ligand networks Cell 2013 154 228 239 10.1016/j.cell.2013.06.006
Ghamsari L. Balaji S. Shen Y. Yang X. Balcha D. Fan C. Hao T. Yu H. Papin J.A. Salehi-Ashtiani K. Genome-wide functional annotation and structural verification of metabolic ORFeome of Chlamydomonas reinhardtii BMC Genom. 2011 12 (Suppl. S1) S4 10.1186/1471-2164-12-S1-S4
Pellet J. Tafforeau L. Lucas-Hourani M. Navratil V. Meyniel L. Achaz G. Guironnet-Paquet A. Aublin-Gex A. Caignard G. Cassonnet P. et al. ViralORFeome: An integrated database to generate a versatile collection of viral ORFs Nucleic Acids Res. 2010 38 D371 D378 10.1093/nar/gkp1000
Fu W. Nelson D.R. Mystikou A. Daakour S. Salehi-Ashtiani K. Advances in microalgal research and engineering development Curr. Opin. Biotechnol. 2019 59 157 164 10.1016/j.copbio.2019.05.013 31252302
