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Symbiotic N2-Fixer Community Composition, but Not Diversity, Shifts in Nodules of a Single Host Legume Across a 2-Million-Year Dune Chronosequence

  • Plant Microbe Interactions
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Abstract

Long-term soil age gradients are useful model systems to study how changes in nutrient limitation shape communities of plant root mutualists because they represent strong natural gradients of nutrient availability, particularly of nitrogen (N) and phosphorus (P). Here, we investigated changes in the dinitrogen (N2)-fixing bacterial community composition and diversity in nodules of a single host legume (Acacia rostellifera) across the Jurien Bay chronosequence, a retrogressive 2 million-year-old sequence of coastal dunes representing an exceptionally strong natural soil fertility gradient. We collected nodules from plants grown in soils from five chronosequence stages ranging from very young (10s of years; associated with strong N limitation for plant growth) to very old (> 2,000,000 years; associated with strong P limitation), and sequenced the nifH gene in root nodules to determine the composition and diversity of N2-fixing bacterial symbionts. A total of 335 unique nifH gene operational taxonomic units (OTUs) were identified. Community composition of N2-fixing bacteria within nodules, but not diversity, changed with increasing soil age. These changes were attributed to pedogenesis-driven shifts in edaphic conditions, specifically pH, exchangeable manganese, resin-extractable phosphate, nitrate and nitrification rate. A large number of common N2-fixing bacteria genera (e.g. Bradyrhizobium, Ensifer, Mesorhizobium and Rhizobium) belonging to the Rhizobiaceae family (α-proteobacteria) comprised 70% of all raw sequences and were present in all nodules. However, the oldest soils, which show some of the lowest soil P availability ever recorded, harboured the largest proportion of unclassified OTUs, suggesting a unique set of N2-fixing bacteria adapted to extreme P limitation. Our results show that N2-fixing bacterial composition varies strongly during long-term ecosystem development, even within the same host, and therefore rhizobia show strong edaphic preferences.

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References

  1. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215–236. https://doi.org/10.1146/annurev.ecolsys.39.110707.173423

    Article  Google Scholar 

  2. Sprent J, Ardley J, James E (2013) From North to South: a latitudinal look at legume nodulation processes. S Afr J Bot 89:31–41. https://doi.org/10.1016/j.sajb.2013.06.011

    Article  Google Scholar 

  3. The current taxonomy of rhizobia. NZ Rhizobia website. http://www.rhizobia.co.nz/taxonomy/rhizobia Last updated: X Jan, 2016. [Accessed on 20th of Jan, 2016]. (2016). Accessed 12/06/2015

  4. Thrall PH, Slattery JF, Broadhurst LM, Bickford S (2007) Geographic patterns of symbiont abundance and adaptation in native Australian Acacia–rhizobia interactions. J Ecol 95(5):1110–1122. https://doi.org/10.1111/j.1365-2745.2007.01278.x

    Article  Google Scholar 

  5. Thrall PH, Burdon JJ, Woods MJ (2000) Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian legumes: interactions within and between genera. J Appl Ecol 37(1):52–65. https://doi.org/10.1046/j.1365-2664.2000.00470.x

    Article  Google Scholar 

  6. Sherry SP (1971) The Black Wattle (Acacia mearnsii De Wild.). University of Natal Press, Pietermaritzburg

  7. Boddey R, De Oliveira O, Urquiaga S, Reis V, De Olivares F, Baldani V, Döbereiner J (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant Soil 174. https://doi.org/10.1007/978-94-011-0053-3_9

    Chapter  Google Scholar 

  8. Heath KD, Tiffin P (2007) Context dependence in the coevolution of plant and rhizobial mutualists. Proc R Soc B: Biol Sc 274(1620):1905–1912. https://doi.org/10.1098/rspb.2007.0495

    Article  Google Scholar 

  9. Weese DJ, Heath KD, Dentinger BTM, Lau JA (2015) Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69(3):631–642. https://doi.org/10.1111/evo.12594

    Article  CAS  PubMed  Google Scholar 

  10. Simonsen AK, Han S, Rekret P, Rentschler CS, Heath KD, Stinchcombe JR (2015) Short-term fertilizer application alters phenotypic traits of symbiotic nitrogen fixing bacteria. PeerJ 3:e1291. https://doi.org/10.7717/peerj.1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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(11):2435–2441. https://doi.org/10.1038/ismej.2015.54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hollowell A, Regus J, Gano K, Bantay R, Centeno D, Pham J, Lyu J, Moore D, Bernardo A, Lopez G (2016) Epidemic spread of symbiotic and non-symbiotic Bradyrhizobium genotypes across California. Microb Ecol 71(3):700–710. https://doi.org/10.1007/s00248-015-0685-5

    Article  CAS  PubMed  Google Scholar 

  13. Neuhauser C, Fargione JE (2004) A mutualism-parasitism continuum model and its application to plant-mycorrhizae interactions. Ecol Model 177(3–4):337–352. https://doi.org/10.1016/j.ecolmodel.2004.02.010

    Article  Google Scholar 

  14. Van Cauwenberghe J, Michiels J, Honnay O (2015) Effects of local environmental variables and geographical location on the genetic diversity and composition of Rhizobium leguminosarum nodulating Vicia cracca populations. Soil Biol Biochem 90:71–79. https://doi.org/10.1016/j.soilbio.2015.08.001

    Article  CAS  Google Scholar 

  15. Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Ecol 237(2):187–193. https://doi.org/10.1111/j.1574-6968.2004.tb09695.x

    Article  CAS  Google Scholar 

  16. Barrett LG, Bever JD, Bissett A, Thrall PH (2015) Partner diversity and identity impacts on plant productivity in Acacia–rhizobial interactions. J Ecol 103(1):130–142. https://doi.org/10.1111/1365-2745.12336

    Article  Google Scholar 

  17. Ferreira TC, Aguilar JV, Souza LA, Justino GC, Aguiar LF, Camargos LS (2016) pH effects on nodulation and biological nitrogen fixation in Calopogonium mucunoides. Braz J Bot 39(4):1015–1020. https://doi.org/10.1007/s40415-016-0300-0

    Article  Google Scholar 

  18. Slattery JF, Coventry DR (1993) Variation of soil populations of Rhizobium leguminosarum bv. Trifolii and the occurrence of inoculant rhizobia in nodules of subterranean clover after pasture renovation in north-eastern Victoria. Soil Biol Biochem 25(12):1725–1730. https://doi.org/10.1016/0038-0717(93)90176-C

    Article  Google Scholar 

  19. Vuong HB, Thrall PH, Barrett LG (2016) Host species and environmental variation can influence rhizobial community composition. J Ecol 105:540–548. https://doi.org/10.1111/1365-2745.12687

    Article  CAS  Google Scholar 

  20. Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98(4):725–736. https://doi.org/10.1111/j.1365-2745.2010.01664.x

    Article  Google Scholar 

  21. Krüger M, Teste FP, Laliberté E, Lambers H, Coghlan M, Zemunik G, Bunce M (2015) The rise and fall of arbuscular mycorrhizal fungal diversity during ecosystem retrogression. Mol Ecol 24(19):4912–4930. https://doi.org/10.1111/mec.13363

    Article  PubMed  Google Scholar 

  22. Dickie IA, Martínez-García LB, Koele N, Grelet G-A, Tylianakis JM, Peltzer DA, Richardson SJ (2013) Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367(1–2):11–39. https://doi.org/10.1007/s11104-013-1609-0

    Article  CAS  Google Scholar 

  23. Albornoz FE, Lambers H, Turner BL, Teste FP, Laliberté E (2016) Shifts in symbiotic associations in plants capable of forming 2 multiple root symbioses across a long-term soil chronosequence. Ecol Evol 6(8):2368–2377. https://doi.org/10.1002/ece3.2000

    Article  PubMed  PubMed Central  Google Scholar 

  24. Turner BL, Laliberté E (2015) Soil development and nutrient availability along a 2 million-year coastal dune chronosequence under species-rich Mediterranean shrubland in Southwestern Australia. Ecosystems 18(2):287–309. https://doi.org/10.1007/s10021-014-9830-0

    Article  CAS  Google Scholar 

  25. Vitousek PM (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, USA

    Google Scholar 

  26. Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois D, Vitousek PM (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecol 76(5):1407–1424. https://doi.org/10.2307/1938144

    Article  Google Scholar 

  27. Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR (2010) Understanding ecosystem retrogression. Ecol Monogr 80(4):509–529. https://doi.org/10.1890/09-1552.1

    Article  Google Scholar 

  28. Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205(4):1525–1536. https://doi.org/10.1111/nph.13208

    Article  CAS  PubMed  Google Scholar 

  29. Martínez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205(4):1565–1576. https://doi.org/10.1111/nph.13226

    Article  CAS  PubMed  Google Scholar 

  30. Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll KH, Zemunik G, Lambers H (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100(3):631–642. https://doi.org/10.1111/j.1365-2745.2012.01962.x

    Article  CAS  Google Scholar 

  31. McArthur, WM & Bettenay, E (1974) Development and Distribution of Soils of the Swan Coastal Plain, Western Australia. CSIRO, Australia.

  32. Odum EP (1969) The strategy of ecosystem development. In: Ndubisi FO (ed) The ecological design and planning reader. Island Press/Center for Resource Economics, Washington, DC, pp 203–216. doi:https://doi.org/10.5822/978-1-61091-491-8_20

    Chapter  Google Scholar 

  33. Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochem 37(1):63–75. https://doi.org/10.1023/A:1005757218475

    Article  CAS  Google Scholar 

  34. Kitayama K, Mueller-Dombois D (1995) Vegetation changes along gradients of long-term soil development in the Hawaiian montane rainforest zone. Plant Ecol 120(1):1–20. https://doi.org/10.1007/BF00033454

    Article  Google Scholar 

  35. Richardson SJ, Peltzer DA, Allen RB, McGlone MS, Parfitt RL (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139(2):267–276. https://doi.org/10.1007/s00442-004-1501-y

    Article  PubMed  Google Scholar 

  36. Laliberté E, Zemunik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345(6204):1602–1605. https://doi.org/10.1126/science.1256330

    Article  CAS  PubMed  Google Scholar 

  37. Zemunik G, Turner BL, Lambers H, Laliberté E (2016) Increasing plant species diversity and extreme species turnover accompany declining soil fertility along a long-term chronosequence in a biodiversity hotspot. J Ecol 104(3):792–805. https://doi.org/10.1111/1365-2745.12546

    Article  Google Scholar 

  38. Albornoz FE, Teste FP, Lambers H, Bunce M, Murray DC, White NE, Laliberté E (2016) Changes in ectomycorrhizal fungal community composition and declining diversity along a 2-million year soil chronosequence. Mol Ecol 25(19):4919–4929. https://doi.org/10.1111/mec.13778

    Article  CAS  PubMed  Google Scholar 

  39. Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sc 188:25–35. https://doi.org/10.1016/j.plantsci.2012.02.010

    Article  CAS  Google Scholar 

  40. Sprent JI, Raven JA (1985) Evolution of nitrogen-fixing symbioses. Proc R Soc Edinb B Biol Sci 85(3–4):215–237. https://doi.org/10.1017/S0269727000004036

    Article  Google Scholar 

  41. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5(7):539–554. https://doi.org/10.1046/j.1462-2920.2003.00451.x

    Article  CAS  PubMed  Google Scholar 

  42. Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity. Environ Microbiol 13(7):1790–1799. https://doi.org/10.1111/j.1462-2920.2011.02488.x

    Article  CAS  PubMed  Google Scholar 

  43. Groves RH (ed) (1994) Australian vegetation2nd edn. Melbourne, Cambridge University Press

    Google Scholar 

  44. Thrall PH, Bever JD, Slattery JF (2008) Rhizobial mediation of Acacia adaptation to soil salinity: evidence of underlying trade-offs and tests of expected patterns. J Ecol 96(4):746–755. https://doi.org/10.1111/j.1365-2745.2008.01381.x

    Article  Google Scholar 

  45. Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions. Can J Microbiol 38(6):475–484. https://doi.org/10.1139/m92-079

    Article  CAS  Google Scholar 

  46. Lowendorf HS, Alexander M (1983) Identification of Rhizobium phaseoli strains that are tolerant or sensitive to soil acidity. Appl Environ Microbiol 45(3):737–742

    CAS  PubMed  PubMed Central  Google Scholar 

  47. McArthur WM, Bettenay E (1960) The development and distribution of the soils of the Swan Coastal Plain, Western Australia. Soil Publication CSIRO, Australia 16

  48. Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nature Plants 1(5):15050. https://doi.org/10.1038/nplants.2015.50

    Article  CAS  Google Scholar 

  49. Enright NJ, Lamont BB, Miller BP (2005) Anomalies in grasstree fire history reconstructions for south-western Australian vegetation. Austral Ecol 30(6):668–673. https://doi.org/10.1111/j.1442-9993.2005.01509.x

    Article  Google Scholar 

  50. Enright NJ, Fontaine JB, Lamont BB, Miller BP, Westcott VC (2014) Resistance and resilience to changing climate and fire regime depend on plant functional traits. J Ecol 102(6):1572–1581

    Article  Google Scholar 

  51. Hoque MS, Broadhurst LM, Thrall PH (2011) Genetic characterisation of root nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across southeastern Australia. Int J Syst Evol Microbiol 61:299–309. https://doi.org/10.1099/ijs.0.021014-0

    Article  CAS  PubMed  Google Scholar 

  52. Birnbaum C, Bissett A, Thrall PH, Leishman MR (2016) Nitrogen-fixing bacterial communities in invasive legume nodules and associated soils are similar across introduced and native range populations in Australia. J Biogeogr 43(8):1631–1644. https://doi.org/10.1111/jbi.12752

    Article  Google Scholar 

  53. Hill Y (2015) Investigation of the symbiotic associations of Acacia ligulata Benth. and Acacia tetragonophylla F.Muell: the potential for use in the rehabilitation of excavated sites at Shark Bay Salt Pty. Ltd. PhD Thesis. Murdoch University, Perth, PerthAustralia

  54. Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102(2):396–410. https://doi.org/10.1111/1365-2745.12196

    Article  CAS  Google Scholar 

  55. Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 55(10):2522–2526

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  58. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  Google Scholar 

  59. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217

    Article  CAS  Google Scholar 

  60. Gaby JC, Buckley DH (2014) A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria. Database 2014:bau001

  61. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32(4):1363–1371. https://doi.org/10.1093/nar/gkh293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26(1):32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x

    Article  Google Scholar 

  63. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

  64. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Peter Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2:4–3 http://CRAN.R-project.org/package=vegan

    Google Scholar 

  65. Cáceres MD, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90(12):3566–3574. https://doi.org/10.1890/08-1823.1

    Article  PubMed  Google Scholar 

  66. Venables WN, Ripley BD (2002) Modern applied statistics with SFourth edn. Springer, New York

    Book  Google Scholar 

  67. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  68. Hope RM (2013) Rmisc: Ryan miscellaneous. R package version 1:5

    Google Scholar 

  69. Navarro DJ (2015) Learning statistics with R: a tutorial for psychology students and other beginners. (Version 0.5). University of Adelaide, Adelaide, Australia

  70. Taylor SR, McLennan SM (1985) The continental crust: its composition and evolution, vol 1. Blackwell Press, Oxford

    Google Scholar 

  71. Chen CR, Hou EQ, Condron LM, Bacon G, Esfandbod M, Olley J, Turner BL (2015) Soil phosphorus fractionation and nutrient dynamics along the Cooloola coastal dune chronosequence, southern Queensland, Australia. Geoderma 257-258(supplement C):4–13. https://doi.org/10.1016/j.geoderma.2015.04.027

    Article  CAS  Google Scholar 

  72. Png GK, Turner BL, Albornoz FE, Hayes PE, Lambers H, Laliberté E (2017) Greater root phosphatase activity in nitrogen-fixing rhizobial but not actinorhizal plants with declining phosphorus availability. J Ecol n/a:n/a 105:1246–1255. https://doi.org/10.1111/1365-2745.12758

    Article  CAS  Google Scholar 

  73. Krasova-Wade T, Diouf O, Ndoye I, Sall CE, Braconnier S, Neyra M (2006) Water-condition effects on rhizobia competition for cowpea nodule occupancy. Afr J Biotechnol 5(16):1457–1463

    CAS  Google Scholar 

  74. Brockwell J, Pilka A, Holliday R (1991) Soil pH is a major determinant of the numbers of naturally occurring Rhizobium meliloti in non-cultivated soils in central New South Wales. Austr J Exp Agr 31(2):211–219. https://doi.org/10.1071/EA9910211

    Article  Google Scholar 

  75. West S, Kiers ET, Pen I, Denison R (2002) Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J Evol Biol 15(5):830–837. https://doi.org/10.1046/j.1420-9101.2002.00441.x

    Article  Google Scholar 

  76. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Ann Rev Ecol System 19:207–233. https://doi.org/10.1146/annurev.es.19.110188.001231

    Article  Google Scholar 

  77. Cooper VS, Lenski RE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407(6805):736–739. https://doi.org/10.1038/35037572

    Article  CAS  PubMed  Google Scholar 

  78. Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martínez-Romero E, Werner D (2003) Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol plant-microbe inter 16(2):159–168. https://doi.org/10.1094/MPMI.2003.16.2.159

    Article  CAS  Google Scholar 

  79. Martyniuk S, Oron J, Martyniuk M (2005) Diversity and numbers of root-nodule bacteria [rhizobia] in Polish soils. Acta Soc Bot Pol 74(1):83–86

    Article  Google Scholar 

  80. Wielbo J, Kidaj D, Koper P, Kubik-Komar A, Skorupska A (2012) The effect of biotic and physical factors on the competitive ability of Rhizobium leguminosarum. Open Life Sci 7(1):13–24

    CAS  Google Scholar 

  81. Provorov NA, Vorobyov NI (2006) Interplay of Darwinian and frequency-dependent selection in the host-associated microbial populations. Theor Pop Biol 70(3):262–272. https://doi.org/10.1016/j.tpb.2006.06.002

    Article  Google Scholar 

  82. Sachs J, Kembel S, Lau A, Simms E (2009) In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Appl Environ Microbiol 75(14):4727–4735

    Article  CAS  Google Scholar 

  83. Turk D, Keyser HH (1992) Rhizobia that nodulate tree legumes: specificity of the host for nodulation and effectiveness. Can J Microbiol 38(6):451–460. https://doi.org/10.1139/m92-076

    Article  Google Scholar 

  84. Lodeiro AR, Favelukes G (1999) Early interactions of Bradyrhizobium japonicum and soybean roots: specificity in the process of adsorption. Soil Biol Biochem 31(10):1405–1411. https://doi.org/10.1016/S0038-0717(99)00058-9

    Article  CAS  Google Scholar 

  85. Lieven-Antoniou C, Whittam T (1997) Specificity in the symbiotic association of Lotus corniculatus and Rhizobium loti from natural populations. Mol Ecol 6(7):629–639. https://doi.org/10.1046/j.1365-294X.1997.00224.x

    Article  CAS  Google Scholar 

  86. Walker T, Syers J (1976) The fate of phosphorus during pedogenesis. Geoderma 15(1):1–19. https://doi.org/10.1016/0016-7061(76)90066-5

    Article  CAS  Google Scholar 

  87. Batterman SA, Wurzburger N, Hedin LO (2013) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101(6):1400–1408. https://doi.org/10.1111/1365-2745.12138

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Yvette Hill who provided comments and information of rhizobia nodulating A. rostellifera. We appreciate the cooperation by the Western Australian Department of Parks and Wildlife (DPaW) with acquiring permits to sample the field soils. We are grateful for the hard work of Yuphin Khentry and Ghulam Abbas during the soil collections and glasshouse measurements.

Funding

This research was made possible by research grants from the Australian Research Council (DE120100352 and DP130100016) and the Hermon Slade Foundation to E.L.

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Author notes

  1. Christina Birnbaum

    Present address: Department of Ecology and Evolutionary Biology, School of Science and Engineering, Tulane University, 6823 St Charles Ave, New Orleans, LA, 70118, USA

Authors and Affiliations

  1. Environmental and Conservation Sciences, School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Perth, Western Australia, 6150, Australia

    Christina Birnbaum

  2. CSIRO Oceans and Atmosphere, Hobart, Australia

    Andrew Bissett

  3. Grupo de Estudios Ambientales, IMASL-CONICET & Universidad Nacional de San Luis, Av. Ejercito de los Andes 950, 5700, San Luis, Argentina

    Francois P. Teste

  4. School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, (Perth), Western Australia, 6009, Australia

    Francois P. Teste & Etienne Laliberté

  5. Centre sur la biodiversité, Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal, 4101 Sherbrooke Est, Montréal, Quebec, H1X 2B2, Canada

    Etienne Laliberté

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Contributions

FPT and EL designed the experiment. FPT supervised and maintained the experiment. CB conducted the DNA extractions. CB performed statistical analyses with assistance from all authors. AB conducted the bioinformatics work. CB led the writing of the manuscript and all authors contributed to revisions.

Corresponding author

Correspondence to Christina Birnbaum.

Electronic Supplementary Material

Online resource 1

List of 30 soil variables, sampling levels and methods used in dbRDA analyses. (XLSX 13 kb)

Online resource 2

Means and ± S.E. of 30 soil variables used in the dbRDA analysis. (XLSX 13 kb)

ESM 1

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Phylogenetic tree showing the 335 OTUs based on nifH gene amplified from A. rostellifera nodules’ DNA after growing in the greenhouse in soils collected across five chronosequence stages in Jurien Bay, Western Australia. The tree is based on the neighbour joining tree of Gaby et al. (2014) to which 335 OTU sequences were added using the ARB parsimony tool. Three phylogenetically distinct clusters are shown. In blue are marked the 12 most common OTUs based on Table 2. In green are marked OTUs that associated significantly with dune stage 5 (the oldest) based on Table 3. (attached separately) (PDF 50 kb)

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Birnbaum, C., Bissett, A., Teste, F.P. et al. Symbiotic N2-Fixer Community Composition, but Not Diversity, Shifts in Nodules of a Single Host Legume Across a 2-Million-Year Dune Chronosequence. Microb Ecol 76, 1009–1020 (2018). https://doi.org/10.1007/s00248-018-1185-1

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  • DOI: https://doi.org/10.1007/s00248-018-1185-1

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