Abstract
The ability to fix nitrogen is widely, but sporadically distributed among the Bacteria and Archaea suggesting either a vertically inherited, ancient function with widespread loss across genera or an adaptive feature transferred laterally between co-inhabitants of nitrogen-poor environments. As previous phylogenetic studies of nifH and nifD have not completely resolved the evolutionary history of nitrogenase, sixty nifD, nifK, and combined nifDK genes were analyzed using Bayesian, maximum likelihood, and parsimony algorithms to determine whether the individual and combined datasets could provide additional information. The results show congruence between the 16S and nifDK phylogenies at the phyla level and generally support vertical descent with loss. However, statistically significant differences between tree topographies suggest a complex evolutionary history with the underlying pattern of vertical descent obscured by recurring lateral transfer events and different patterns of evolution between the genes. Results support inheritance from the Last Common ancestor or an ancient lateral transfer of the nif genes between Bacteria and Archaea, ongoing gene transfer between cohabitants of similar biogeographic regions, acquisition of nitrogen-fixing capability via symbiosis islands, possible xenologous displacement of one gene in the operon, and possible retention of ancestral genes in heterocystous cyanobacteria. Analyses support the monophyly of the Cyanobacteria, αβγ-Proteobacteria, and Actinobacteria (Frankia) and provide strong support for the placement of Frankia nif genes at the base of combined the Cyanobacteria/Proteobacteria clades.
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References
Adams DG (2000) Heterocyst formation in cyanobacteria. Curr Opin Microbiol 3:618–624
Baar C, Eppinger M, Raddatz G, Simon J, Lanz C, Klimmek O, Nandakumar R, Gross R, Rosinus A, Keller H et al (2003) Complete genome sequence and analysis of Wolinella succinogenes. PNAS 100:11690–11695
Bergman B, Rasmussen U, Rai AN (2007) Cyanobacterial associations. In: Newton WE, Elmerich C (eds) Associative and endophytic nitrogen-fixing bacteria and Cyanobacterial associations. Kluwer Academic, Dordrecht, pp 257–301
Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154:157–164
Brown JM, Lemmon AR (2007) The importance of data partitioning and the utility of bayes factors in bayesian phylogenetics. Syst Biol 56:643–655
Cantera JJL, Kawasaki H, Seki T (2004) The nitrogen-fixing gene (nifH) of Rhodopseudomonas palustris: a case of lateral gene transfer? Microbiology 150:2237–2246
Castenholz RW (2001) Phylum BX. Cyanobacteria, oxygenic photosynthetic bacteria. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, Second edn. Springer, New York, pp 473–599
Chen W-M, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-Proteobacteria is widespread in nature. J Bacteriol 185:7266–7272
Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:D169–D172
Dean DR, Jacobson MR (1992) Biochemical genetics of nitrogenase. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 793–834
Dedysh SN, Ricke P, Liesack W (2004) NifH and NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria. Microbiology 150:1301–1313
Enkh-Amgalan J, Kawasaki H, Seki T (2005) NifH and NifD sequences of Heliobacteria: a new lineage in the nitrogenase phylogeny. FEMS Lett 243:73–79
Enkh-Amgalan J, Kawasaki H, Seki T (2006) Molecular evolution of the nif gene cluster carrying nifI 1 and nifI 2 genes in the gram-positive phototrophic bacterium Heliobacterium chlorum. Int J Syst Evol Micro 56:65–74
Fani R, Gallo R, Liò P (2000) Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. J Mol Evol 51:1–11
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Garrity GM, Holt JG (2001) Phylum BXIII firmicutes. In: Boone DR, Castenholzb RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 625–630
Haselkorn R, Buikema WJ (1992) Nitrogen fixation in cyanobacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 166–190
Hennecke H, Kaluza K, Thöny M, Fuhrmann M, Ludwig W, Stackebrandt E (1985) Concurrent evolution of nitrogenase genes and 16S rRNA in Rhizobium species and other nitrogen fixing bacteria. Arch Microbiol 142:342–348
Henson BJ, Watson LE, Barnum SR (2002) Molecular differentiation of the heterocystous cyanobacteria, Nostoc and Anabaena, based on complete NifD sequences. Curr Microbiol 45:161–164
Henson BJ, Hesselbrock SM, Watson LE, Barnum SR (2004a) Molecular phylogeny of the heterocystous cyanobacteria (Subsections IV and V) based on nifD. Int J Syst Evol Microbiol 54:493–497
Henson BJ, Watson LE, Barnum SR (2004b) The evolutionary history of nitrogen fixation, as assessed by NifD. J Mol Evol 58:390–399
Hirsch AM, McKhann HI, Reddy A, Liao J, Fang Y, Marshall CR (1995) Assessing horizontal transfer of nifHDK genes in eubacteria: nucleotide sequence of nifK from Frankia strain HFPCc13. Mol Biol Evol 12:16–27
Holmes DE, Nevin KP, Lovley DR (2004) Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov. Int J Syst Evol Microbiol 54:1591–1599
Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hurek T, Egener T, Reinhold-Hurek B (1997) Divergence in nitrogenases of Azoarcus spp., Proteobacteria of the β subclass. J Bacteriol 179:4172–4178
Iteman I, Rippka R, Tandeau de Marsac N, Herdman M (2002) rDNA analyses of planktonic heterocystous cyanobacteria including members of the genera Anabaenopsis and Cyanospira. Microbiology 148:481–496
Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 96:3801–3806
Jobb GA, vonHaeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:I8
Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K et al (2002) Complete genomic sequence of nitrogen-fixing symbiotic Bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197
Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795
Kneip C, Vob C, Lockhart PJ, Maier UG (2008) The cyanobacterial endosymbiont of the unicelluar algae Rhopalodia gibba shows reductive genome evolution. BMC Evol Biol 8(30):1–16
Ludwig W, Klenk H-P (2001) Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systematics. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer-Verlag, New York, pp 49–65
Morrison DA, Ellis JT (1997) Effects of nucleotide sequence alignment on phylogeny estimation: a case study of 18S rDNAs of Apicomplexa. Mol Biol Evol 14:428–441
Navarro-González R, McKay CP, Mvondo DN (2001) A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightening. Nature 412:61–64
Newton WE (1997) Molybdenum-nitrogenase: structure and function. In: Legocki H, Bothe E, Pühler A (eds) Biological nitrogen for ecology and sustainable agriculture, Springer-Verlag, Berlin, pp 9–12
Normand P, Bousquet J (1989) Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol 29:436–447
Normand P, Gouy M, Cournoyer B, Simonet P (1992) Nucleotide sequence of nifD from Frankia alni strain Arl3: phylogenic inferences. Mol Biol Evol 9:495–506
Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67
Omelchenko MV, Makarova KS, Wolf YI, Rogozin IB, Koonin EV (2003) Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol 4:R55
Parker MA, Lafay B, Burdon JJ, van Berkum P (2002) Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium. Microbiology 148:2557–2565
Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W700–W703
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Posada D, Crandall KA (2001) Selecting the best-fit model of nucleotide substitution. Systems Biol 50:580–601
Postgate JR (1982) The fundamentals of nitrogen fixation. Cambridge University Press, New York
Postgate JR (1992) The Leeuwenhoek lecture, 1992 Bacterial evolution and the nitrogen-fixing plant. Philos Trans R Soc B 338:409–416
Postgate JR (1998) Nitrogen fixation, 3rd edn. Cambridge University Press, Cambridge
Postgate JR, Eady RR (1988) The evolution of biological nitrogen fixation. In: Bothe H, de Bruijn FJ, Newton WE (eds) Nitrogen fixation: one hundred years after. Gustav Fischer, New York
Qian J, Parker MA (2002) Contrasting nifD and ribosomal gene relationships among Mesorhizobium from Lotus oroboides in Northern Mexico. Syst Appl Microbiol 25:68–73
Qian J, Kwon S-W, Parker MA (2003) rRNA and nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiol Lett 219:159–165
Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554
Riedel GE, Brown SE, Ausubel FM (1983) Nitrogen fixation by Klebsiella pneumoniae is inhibited by certain multicopy hybrid nif plasmids. J Bacteriol 153:45–56
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 110:1–61
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95:5145–5149
Sur S, Sen A, Bothra AK (2007) Mutational drift prevails over translational efficiency in Frankia nif operons. Indian J Biotech 6:321–328
Swofford D (2002) PAUP* 4.0: phylogenetic analysis using parsimony. Sinauer Associates, Sunderland
Thiel T, Lyons EM, Erker JC, Ernst A (1995) A second nitrogenase in vegetative cells of a heterocystous-forming cyanobacterium. Proc Natl Acad Sci USA 92:9358–9362
Thiel T, Lyons EM, Erker JC (1997) Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis. J Bacteriol 179:5222–5225
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Turner S (1997) Molecular systematics of oxygenic photosynthetic bacteria. Plant Syst Evol (Suppl) 11:13–52
Weinman JJ, Fellows FF, Gresshoff PM, Shine J, Scott KF (1984) Structural analysis of the genes encoding the molybdenum-iron protein of nitrogenase in the Parasponia rhizobium strain ANU289. Nucleic Acids Res 12:8329–8344
Wilmotte A, Herdman M (2001) Phylogenetic relationships among the cyanobacteria based on 16s rRNA sequences. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, Second edn. Springer, Heidelberg, pp 487–493
Wilmotte A, Turner S, Van de Peer Y, Pace NR (1992) Taxonomic study of marine oscillatoriacean strains (cyanobacteria) with narrow trichomes. II. Nucleotide sequence analysis of the 16S ribosomal RNA. J Phycol 28:828–838
Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, Lu W, Zhang W, Yao Z, Li H et al (2008) Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. PNAS 105:7564–7569
Young JPW (1992) Phylogenetic classification of nitrogen-fixing organisms. In: Stacey G, Burris RH, Evans HJ (eds) Biological Nitrogen Fixation. Chapman & Hall, New York, pp 43–86
Zehr JP, Mellon MT, Hiorns WD (1997) Phylogeny of cyanobacterial nifH genes: evolutionary implications and potential applications to natural assemblages. Microbiology 143:1443–1450
Zehr JP, Mellon MT, Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Environ Microb 64:3444–3450
Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554
Acknowledgments
A Department of Botany Academic Challenge Grant to L.S.H. funded this research in part. We wish to acknowledge the help of Eric Tepe in developing the initital Mr. Bayes analyses and to The Center for Functional Genomics and Bioinformatics at Miami University for assistance with sequencing.
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Hartmann, L.S., Barnum, S.R. Inferring the Evolutionary History of Mo-Dependent Nitrogen Fixation from Phylogenetic Studies of nifK and nifDK . J Mol Evol 71, 70–85 (2010). https://doi.org/10.1007/s00239-010-9365-8
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DOI: https://doi.org/10.1007/s00239-010-9365-8