{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,10]],"date-time":"2026-04-10T18:08:55Z","timestamp":1775844535210,"version":"3.50.1"},"reference-count":51,"publisher":"Oxford University Press (OUP)","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2012,3,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Motivation: Fixed nitrogen is an essential requirement for the biosynthesis of cellular nitrogenous compounds. Some cyanobacteria can fix nitrogen, contributing significantly to the nitrogen cycle, agriculture and biogeochemical history of Earth. The rate and position on the species phylogeny of gains and losses of this ability, as well as of the underlying nif genes, are controversial.<\/jats:p>\n               <jats:p>Results: We use probabilistic models of trait evolution to investigate the presence and absence of cyanobacterial nitrogen-fixing ability. We estimate rates of change on the species phylogeny, pinpoint probable changes and reconstruct the state and nif gene complement of the ancestor. Our results are consistent with a nitrogen-fixing cyanobacterial ancestor, repeated loss of nitrogen fixation and vertical descent, with little horizontal transfer of the genes involved.<\/jats:p>\n               <jats:p>Contact: \u00a0db60@st-andrews.ac.uk<\/jats:p>\n               <jats:p>Supplementary information: \u00a0Supplementary data are available at Bioinformatics online.<\/jats:p>","DOI":"10.1093\/bioinformatics\/bts008","type":"journal-article","created":{"date-parts":[[2012,1,12]],"date-time":"2012-01-12T03:10:30Z","timestamp":1326337830000},"page":"603-606","source":"Crossref","is-referenced-by-count":95,"title":["The evolution of nitrogen fixation in cyanobacteria"],"prefix":"10.1093","volume":"28","author":[{"given":"Natasha","family":"Latysheva","sequence":"first","affiliation":[{"name":"1 Centre for Evolution, Genes and Genomics, School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK, 2Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK and 3Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK"}]},{"given":"Vivien L.","family":"Junker","sequence":"additional","affiliation":[{"name":"1 Centre for Evolution, Genes and Genomics, School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK, 2Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK and 3Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK"}]},{"given":"William J.","family":"Palmer","sequence":"additional","affiliation":[{"name":"1 Centre for Evolution, Genes and Genomics, School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK, 2Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK and 3Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK"},{"name":"1 Centre for Evolution, Genes and Genomics, School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK, 2Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK and 3Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK"}]},{"given":"Geoffrey A.","family":"Codd","sequence":"additional","affiliation":[{"name":"1 Centre for Evolution, Genes and Genomics, School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK, 2Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK and 3Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK"}]},{"given":"Daniel","family":"Barker","sequence":"additional","affiliation":[{"name":"1 Centre for Evolution, Genes and Genomics, School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK, 2Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK and 3Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK"}]}],"member":"286","published-online":{"date-parts":[[2012,1,11]]},"reference":[{"key":"2023012512191341300_B1","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: a new generation of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"2023012512191341300_B2","doi-asserted-by":"crossref","first-page":"e3","DOI":"10.1371\/journal.pcbi.0010003","article-title":"Predicting functional gene links from phylogenetic-statistical analyses of whole genomes","volume":"1","author":"Barker","year":"2005","journal-title":"PLoS Comput. 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Microbiol."},{"key":"2023012512191341300_B5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1472-4669.2009.00220.x","article-title":"Timing of morphological and ecological innovations in the cyanobacteria \u2013 a key to understanding the rise in atmospheric oxygen","volume":"8","author":"Blank","year":"2010","journal-title":"Geobiology"},{"key":"2023012512191341300_B6","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1111\/j.1472-4669.2011.00278.x","article-title":"A late methanogen origin for molybdenum-dependent nitrogenases","volume":"9","author":"Boyd","year":"2011","journal-title":"Geobiology"},{"key":"2023012512191341300_B7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0303-2647(83)90021-7","article-title":"Nitrogen fixation as evidence for the reducing nature of the early biosphere","volume":"16","author":"Broda","year":"1983","journal-title":"Biosystems"},{"key":"2023012512191341300_B8","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1080\/10635150600697465","article-title":"Evolutionary history of vegetative reproduction in Porpidia s.l. (lichen-forming Ascomycota)","volume":"55","author":"Buschbom","year":"2006","journal-title":"Syst. Biol."},{"key":"2023012512191341300_B9","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1126\/science.1061976","article-title":"Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth","volume":"293","author":"Catling","year":"2001","journal-title":"Science"},{"key":"2023012512191341300_B10","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.taap.2004.02.016","article-title":"Cyanobacterial toxins: risk management for health protection","volume":"203","author":"Codd","year":"2005","journal-title":"Toxicol. Appl. Pharm."},{"key":"2023012512191341300_B11","doi-asserted-by":"crossref","first-page":"3019","DOI":"10.1093\/molbev\/msr108","article-title":"Large-scale phylogenomic analyses indicate a deep origin of primary plastids within Cyanobacteria","volume":"28","author":"Criscuolo","year":"2011","journal-title":"Mol. Biol. 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Micr."},{"key":"2023012512191341300_B17","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1111\/j.1365-313X.2008.03492.x","article-title":"Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances","volume":"54","author":"Hu","year":"2008","journal-title":"Plant J."},{"key":"2023012512191341300_B18","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1080\/10635150390192780","article-title":"Stochastic mapping of morphological characters","volume":"52","author":"Huelsenbeck","year":"2003","journal-title":"Syst. Biol."},{"key":"2023012512191341300_B19","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S0168-1656(01)00334-0","article-title":"Cyanobacteria in Uruguayan rice fields: diversity, nitrogen fixing ability and tolerance to herbicides and combined nitrogen","volume":"91","author":"Irisarri","year":"2001","journal-title":"J. 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Proceedings of the 7th International Congress on Nitrogen Fixation.","author":"Postgate","year":"1988"},{"key":"2023012512191341300_B37","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1046\/j.1469-8137.1998.00168.x","article-title":"The past, present and future of nitrogenous compounds in the atmosphere, and their interactions with plants","volume":"139","author":"Raven","year":"1998","journal-title":"New Phytol."},{"key":"2023012512191341300_B38","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1093\/molbev\/msh047","article-title":"The natural history of nitrogen fixation","volume":"21","author":"Raymond","year":"2004","journal-title":"Mol. Biol. Evol."},{"key":"2023012512191341300_B39","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1073\/pnas.77.1.191","article-title":"Interspecies homology of nitrogenase genes","volume":"77","author":"Ruvkun","year":"1980","journal-title":"Proc. Natl Acad. Sci. 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Evol."},{"key":"2023012512191341300_B45","doi-asserted-by":"crossref","first-page":"5442","DOI":"10.1073\/pnas.0600999103","article-title":"The evolutionary diversification of cyanobacteria: Molecular-phylogenetic and paleontological perspectives","volume":"103","author":"Tomitani","year":"2006","journal-title":"Proc. Natl Acad. Sci. 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