Metapopulation dominance and genomicisland acquisition of Bradyrhizobium with superior catabolic capabilities

Proceedings of the Royal Society B: Biological Sciences

Volumn 283, Issue 1829, 2016, Pages

  Hollowell, Amanda C ^a   Regus, John U ^a   Turissini, David ^b   Gano Cohen, Kelsey A ^a   Bantay, Roxanne ^a   Bernardo, Andrew ^a   Moore, Devora ^a   Pham, Jonathan ^a   Sachs, Joel L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Epidemic; Fitness; Genomic island; Rhizobia; Selective sweep; Symbiont

Indexed keywords

ABUNDANCE; CARBON; CATABOLISM; CHROMOSOME; DOMINANCE; EPIDEMIC; FITNESS; GENE EXPRESSION; GENOMICS; GENOTYPE; HOST PLANT; HOST RANGE; LEGUME; METAPOPULATION; NATIVE SPECIES; PHENOTYPE; RHIZOBACTERIUM; SOIL MICROORGANISM; SPATIAL DISTRIBUTION; SYMBIONT; SYMBIOSIS;

BRADYRHIZOBIUM;

BIOLOGICAL MODEL; BRADYRHIZOBIUM; CARBON CYCLE; CLASSIFICATION; FABACEAE; GENETICS; GENOMIC ISLAND; HAPLOTYPE; HOST RANGE; LOTUS (GENUS); METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; NODULATION; PHYLOGENY; SYMBIOSIS;

BRADYRHIZOBIUM; CARBON CYCLE; EVOLUTION, MOLECULAR; FABACEAE; GENOMIC ISLANDS; HAPLOTYPES; HOST SPECIFICITY; LOTEAE; MODELS, GENETIC; PHYLOGENY; ROOT NODULES, PLANT; SOIL MICROBIOLOGY; SYMBIOSIS;

EID: 84964765856     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2016.0496     Document Type: Article

References (76)

1. Parker MA. 2015 The spread of Bradyrhizobium lineages across host legume clades: from Abarema to Zygia. Microb. Ecol. 69, 630-640.(doi:10.1007/s00248-014-0503-5)
2. VanInsberghe D, Maas KR, Cardenas E, Strachan CR, Hallam SJ, Mohn WW. 2015 Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils. ISME J. 9, 2435-2441.(doi:10.1038/ismej.2015.54)
3. Hollowell AC et al. 2015 Native California soils are selective reservoirs for multidrug-resistant bacteria. Environ. Microbiol. Rep. 7, 442-449.(doi:10.1111/1758-2229.12269)
4. Sachs JL, Kembel SW, Lau AH, Simms EL. 2009 In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Appl. Environ. Microbiol. 75, 4727-4735.(doi:10.1128/AEM.00667-09)
5. Pessi G, Ahrens CH, Rehrauer H, Lindemann A, Hauser F, Fischer H-M, Hennecke H. 2007 Genomewide transcript analysis of Bradyrhizobium japonicum bacteroids in soybean root nodules. Mol. Plant-Microb. Interact. 20, 1353-1363.(doi:10.1094/MPMI-20-11-1353)
6. Uchiumi T et al. 2004 Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J. Bacteriol. 186, 2439-2448.(doi:10.1128/JB.186.8.2439-2448.2004)
7. Kaneko T et al. 2000 Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7, 331-338.(doi:10.1093/dnares/7.6.331)
8. Kaneko T et al. 2002 Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9, 189-197.(doi:10.1093/dnares/9.6.189)
9. Martinez-Abarca F, Martinez-Rodriguez L, Lopez-Contreras JA, Jimenez-Zurdo JI, Toro N. 2013 Complete genome sequence of the alfalfa symbiont Sinorhizobium/Ensifer meliloti strain GR4. Genome Announcements 1, e00174-12.(doi:10.1128/genomeA.00174-12)
10. Young JPW et al. 2006 The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7, R34.(doi:10.1186/gb-2006-7-4-r34)
11. McInnes A, Thies JE, Abbott LK, Howieson JG. 2004 Structure and diversity among rhizobial strains, populations and communities: a review. Soil Biol. Biochem. 36, 1295-1308.(doi:10.1016/j.soilbio.2004.04.011)
12. Hollowell AC et al. 2016 Epidemic spread of symbiotic and non-symbiotic Bradyrhizobium genotypes across California. Microb. Ecol. 71, 700-710.(doi:10.1007/s00248-015-0685-5)
13. Epstein B et al. 2012 Population genomics of the facultatively mutualistic bacteria Sinorhizobium meliloti and S. medicae. PLoS Genet. 8, e1002868.(doi:10.1371/journal.pgen.1002868)
14. Denison RF. 2000 Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156, 567-576.(doi:10.1086/316994)
15. Douglas AE. 2010 The symbiotic habit. Princeton, NJ: Princeton University Press.
16. Mueller UG, Sachs JL. 2015 Engineering microbiomes to improve plant and animal health. Trends Microbiol. 23, 606-617.(doi:10.1016/j.tim.2015.07.009)
17. Sachs JL, Skophammer RG, Regus JU. 2011 Evolutionary transitions in bacterial symbiosis. Proc. Natl Acad. Sci. USA 108, 10800-10807.(doi:10.1073/pnas.1100304108)
18. Koppell JH, Parker MA. 2012 Phylogenetic clustering of Bradyrhizobium symbionts on legumes indigenous to North America. Microbiology 158, 2050-2059.(doi:10.1099/mic.0.059238-0)
19. Parker MA. 2012 Legumes select symbiosis island sequence variants in Bradyrhizobium. Mol. Ecol. 21, 1769-1778.(doi:10.1111/j.1365-294X.2012.05497.x)
20. Kiers ET, Rousseau RA, West SA, Denison RF. 2003 Host sanctions and the legume-rhizobium mutualism. Nature 425, 78-81.(doi:10.1038/nature01931)
21. Regus JU, Gano KA, Hollowell AC, Sachs JL. 2014 Efficiency of partner choice and sanctions in lotus is not altered by nitrogen fertilization. Proc. R. Soc. B 281, 20132587.(doi:10.1098/rspb.2013.2587)
22. Sachs JL, Russell JE, Lii YE, Black KC, Lopez G, Patil AS. 2010 Host control over infection and proliferation of a cheater symbiont. J. Evol. Biol. 23, 1919-1927.(doi:10.1111/j.1420-9101.2010.02056.x)
23. Simms EL, Taylor DL, Povich J, Shefferson RP, Sachs JL, Urbina M, Tausczik Y. 2006 An empirical test of partner choice mechanisms in a wild legumerhizobium interaction. Proc. R. Soc. B 273, 77-81.(doi:10.1098/rspb.2005.3292)
24. Denison RF, Kiers ET. 2004 Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol. Lett. 237, 187-193.(doi:10.1111/j.1574-6968.2004.tb09695.x)
25. Perrineau MM, Le Roux C, de Faria SM, de Carvalho Balieiro F, Galiana A, Prin Y, Béna G. 2011 Genetic diversity of symbiotic Bradyrhizobium elkanii populations recovered from inoculated and noninoculated Acacia mangium field trials in Brazil. Syst. Appl. Microbiol. 34, 376-384.(doi:10.1016/j.syapm.2011.03.003)
26. Tang J, Bromfield ESP, Rodrigue N, Cloutier S, Tambong JT. 2012 Microevolution of symbiotic Bradyrhizobium populations associated with soybeans in east North America. Ecol. Evol. 2, 2943-2961.(doi:10.1002/ece3.404)
27. Triplett EW, Sadowsky MJ. 1992 Genetics of competition for nodulation of legumes. Annu. Rev. Microbiol. 46, 399-428.(doi:10.1146/annurev.mi.46.100192.002151)
28. Vlassak K, Vanderleyden J, Franco A. 1996 Competition and persistence of Rhizobium tropici and Rhizobium etli in tropical soil during successive bean (Phaseolus vulgaris L.) cultures. Biol. Fertil. Soils 21, 61-68.(doi:10.1007/BF00335994)
29. Parker MA. 2000 Divergent Bradyrhizobium symbionts on Tachigali versicolor from Barro Colorado Island, Panama. Syst. Appl. Microbiol. 23, 585-590.(doi:10.1016/S0723-2020(00)80034-X)
30. Vinuesa P, Rademaker JLW, de Bruijn FJ, Werner D. 1998 Genotypic characterization of Bradyrhizobium strains nodulating endemic woody legumes of the Canary Islands by PCR-restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rDNA) and 16S-23S rDNA intergenic spacers, repetitive extragenic palindromic PCR genomic fingerprinting, and partial 16S rDNA sequencing. Appl. Environ. Microbiol. 64, 2096-2104.
31. Vinuesa P, Rojas-Jimenez K, Contreras-Moreira B, Mahna SK, Prasad BN, Moe H, Selvaraju SB, Thierfelder H, Werner D. 2008 Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the Asiatic Continent. Appl. Environ. Microbiol. 74, 6987-6996.(doi:10.1128/AEM.00875-08)
32. Vinuesa P, Silva C, Werner D, Martinez-Romero E. 2005 Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol. Phylogenet. Evol. 34, 29-54.(doi:10.1016/j.ympev.2004.08.020)
33. Kaneko T, Maita H, Hirakawa H, Uchiike N, Minamisawa K, Watanabe A, Sato S. 2011 Complete genome sequence of the soybean symbiont Bradyrhizobium japonicum Strain USDA6(T). Genes 2, 763-787.(doi:10.3390/genes2040763)
34. Weber KP, Legge RL. 2009 One-dimensional metric for tracking bacterial community divergence using sole carbon source utilization patterns. J. Microbiol. Methods 79, 55-61.(doi:10.1016/j.mimet.2009.07.020)
35. Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW. 1995 Nodulating strains of rhizobium-loti arise through chromosomal symbiotic gene-transfer in the environment. Proc. Natl Acad. Sci. USA 92, 8985-8989.(doi:10.1073/pnas.92.19.8985)
36. Diep BA et al. 2006 Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367, 731-739.(doi:10.1016/S0140-6736(06)68231-7)
37. Juhas M et al. 2007 Sequence and functional analyses of Haemophilus spp. genomic islands. Genome Biol. 8, R237.(doi:10.1186/gb-2007-8-11-r237)
38. Moulin L, Bena G, Boivin-Masson C, Stepkowski T. 2004 Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol. Phylogenet. Evol. 30, 720-732.(doi:10.1016/S1055-7903(03)00255-0)
39. Sachs JL, Ehinger MO, Simms EL. 2010 Origins of cheating and loss of symbiosis in wild Bradyrhizobium. J. Evol. Biol. 23, 1075-1089.(doi:10.1111/j.1420-9101.2010.01980.x)
40. Silva C, Vinuesa P, Eguiarte LE, Souza V, Martinez-Romero E. 2005 Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol. Ecol. 14, 4033-4050.(doi:10.1111/j.1365-294X.2005.02721.x)
41. Stepkowski T, Czaplinska M, Miedzinska K, Moulin L. 2003 The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst. Appl. Microbiol. 26, 483-494.(doi:10.1078/072320203770865765)
42. Stepkowski T, Moulin L, Krzyzanska A, McInnes A, Law IJ, Howieson J. 2005 European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl. Environ. Microbiol. 71, 7041-7052.(doi:10.1128/AEM.71.11.7041-7052.2005)
43. van Berkum P, Fuhrmann JJ. 2000 Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int. J. Syst. Evol. Microbiol. 50, 2165-2172.(doi:10.1099/00207713-50-6-2165)
44. Sievers F et al. 2011 Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539.(doi:10.1038/msb.2011.75)
45. Darriba D, Taboada GL, Doallo R, Posada D. 2012 jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772.(doi:10.1038/nmeth.2109)
46. Guindon S, Gascuel O. 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.(doi:10.1080/10635150390235520)
47. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010 New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321.(doi:10.1093/sysbio/syq010)
48. Anisimova M, Gascuel O. 2006 Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55, 539-552.(doi:10.1080/10635150600755453)
49. Shimodaira H, Hasegawa M. 1999 Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16, 1114-1116.(doi:10.1093/oxfordjournals.molbev.a026201)
50. Charleston MA. 1998 Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Math. Biosci. 149, 191-223.(doi:10.1016/S0025-5564(97)10012-8)
51. Stamatakis A, Auch AF, Meier-Kolthoff J, Goeker M. 2007 AxPcoords & parallel AxParafit: statistical cophylogenetic analyses on thousands of taxa. BMC Bioinform. 8, 405.(doi:10.1186/1471-2105-8-405)
52. Meier-Kolthoff JP, Auch AF, Huson DH, Goeker M. 2007 CopyCat: cophylogenetic analysis tool. Bioinformatics 23, 898-900.(doi:10.1093/bioinformatics/btm027)
53. 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.(doi:10.1073/pnas.95.9.5145)
54. Nei M. 1987 Molecular evolutionary genetics. New York, NY: Columbia University Press.
55. Tajima F. 1983 Evolutionary relationship of DNAsequences in finite populations. Genetics 105, 437-460.
56. Kimura M. 1977 Preponderance of synonymous changes as evidence for neutral theory of molecular evolution. Nature 267, 275-276.(doi:10.1038/267275a0)
57. Lewontin RC. 1964 Interaction of selection þ linkage. I. General considerations—heterotic models. Genetics 49, 49-67.
58. Hudson RR. 1987 Estimating the recombination parameter of a finite population-model without selection. Genet. Res. 50, 245-250.(doi:10.1017/S0016672300023776)
59. Hudson RR, Kaplan NL. 1985 Statistical properties of the number of recombination events in the history of a sample of DNA-sequences. Genetics 111, 147-164.
60. Weir BS, Cockerham CC. 1984 Estimating F-statistics for the analysis of population-structure. Evolution 38, 1358-1370.(doi:10.2307/2408641)
61. Mantel N. 1967 Detection of disease clustering and a generalized regression approach. Cancer Res. 27, 209-220.
62. Rosenberg MS, Anderson CD. 2011 PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods Ecol. Evol. 2, 229-232.(doi:10.1111/j.2041-210X.2010.00081.x)
63. Librado P, Rozas J. 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.(doi:10.1093/bioinformatics/btp187)
64. Maddison DR, Maddison WP. 2005 MacClade 4.08: analysis of phylogeny and character evolution. Sunderland, MA: Sinauer Associates.
65. Hurlbert SH. 1971 Nonconcept of species diversity—critique and alternative parameters. Ecology 52, 577-586.(doi:10.2307/1934145)
66. Peet RK. 1975 Relative diversity indexes. Ecology 56, 496-498.(doi:10.2307/1934984)
67. Smith JM, Feil EJ, Smith NH. 2000 Population structure and evolutionary dynamics of pathogenic bacteria. Bioessays 22, 1115-1122.(doi:10.1002/1521-1878(200012)22:12,1115::AID-BIES9.3.0.CO;2-R)
68. Smith JM, Smith NH, Orourke M, Spratt BG. 1993 How clonal are bacteria. Proc. Natl Acad. Sci. USA 90, 4384-4388.(doi:10.1073/pnas.90.10.4384)
69. Zak JC, Willig MR, Moorhead DL, Wildman HG. 1994 Functional diversity of microbial communities: a quantitative approach. Soil Biol. Biochem. 26, 1101-1108.(doi:10.1016/0038-0717(94)90131-7)
70. Smith JM, Haigh J. 1974 The hitchhiking effect of a favorable gene. Genet. Res. 23, 23-35.(doi:10.1017/S0016672300014634)
71. Pritchard JK, Pickrell JK, Coop G. 2010 The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 20, R208-R215. (10.1016/j.cub.2009.11.055)
72. Ehinger M, Mohr TJ, Starcevich JB, Sachs JL, Porter SS, Simms EL. 2014 Specialization-generalization trade-off in a Bradyrhizobium symbiosis with wild legume hosts. BMC Ecol. 14, 8.(doi:10.1186/1472-6785-14-8)
73. Croucher NJ et al. 2011 Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430-434.(doi:10.1126/science.1198545)
74. Croucher NJ et al. 2009 Role of conjugative elements in the evolution of the multidrug-resistant pandemic clone Streptococcus pneumoniae (Spain23F) ST81. J. Bacteriol. 191, 1480-1489.(doi:10.1128/JB.01343-08)
75. Kennedy AD et al. 2008 Epidemic communityassociated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc. Natl Acad. Sci. USA 105, 1327-1332.(doi:10.1073/pnas.0710217105)
76. Nazir R, Warmink JA, Boersma H, van Elsas JD. 2010 Mechanisms that promote bacterial fitness in fungalaffected soil microhabitats. FEMS Microbiol. Ecol. 71, 169-185.(doi:10.1111/j.1574-6941.2009.00807.x)