Advertisement

Biological nitrogen fixation by two Acacia species and associated root-nodule bacteria in a suburban Australian forest subjected to prescribed burning

  • 121 Accesses

  • 1 Citations

Abstract

Purpose

Prescribed burning is a forest management practice which can lead to nitrogen (N)-limited conditions. This study aimed to explore whether biological N2 fixation (BNF) remained the main source of N acquisition for two understorey Acacia species in a Eucalyptus-dominated suburban forest of subtropical Australia, 3 to 6 years after prescribed burning. Root-nodule bacteria associated with these acacias were also characterised to unravel the differences in rhizobial communities between sites and species.

Material and methods

Two sites, burned 3 and 6 years before sample collection, were selected within a dry subtropical forest of south-east Queensland, Australia. Leaves were collected from individuals of Acacia disparrima and A. leiocalyx at each site to determine leaf total carbon (C) and N content, C and N isotope composition (δ13C and δ15N) and the percentage of N derived from atmospheric N2. Nodules were harvested from both acacia species at each site to isolate root nodule bacteria. Bacterial isolates were processed for 16S rDNA gene sequencing.

Results and discussion

Generally, no differences were found in plant physiological variables between the two acacia species. Six years after the fire, both species still depended upon BNF for their N supply, with a higher dependence in winter than in summer. Fire, although of low intensity, was likely to have created a N-limited environment which induced the reliance of legumes on BNF. Root nodule bacteria were dominated by non-rhizobial endophytes, mainly from the Firmicutes phylum. No difference in nodule bacterial diversity was found between sites. The relative abundance of rhizobial genera varied amongst plant species and sites, with a shift in dominance from Bradyrhizobium to Rhizobium species between sites 1 and 2.

Conclusions

Our results show that even 6 years after burning, ecosystem remained under N stress and BNF was still the main mechanism for N acquisition by the understorey legumes.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Abdullah KM (2015) – Carbon and nitrogen dynamics following prescribed burning in a suburban native forest of South-east Queensland. Ph.D. thesis, Griffith University. 275 pp

  2. Adams MA, Simon J, Pfautsch S (2010) Woody legumes: a (re)view from the south. Tree Physiol 30:1072–1082

  3. Alves GC, Videira SS, Urquiaga S, Reis VM (2015) Differential plant growth promotion and nitrogen fixation in two genotypes of maize by several Herbaspirillum inoculants. Plant Soil 387:307–321

  4. Amazonas NT, Martinelli LA, Piccolo MC, Rodrigues RR (2011) Nitrogen dynamics during ecosystem development in tropical forest restoration. For Ecol Manag 262:1551–1557

  5. Andreolli M, Lampis S, Zapparoli G, Angelini E, Vallini G (2016) Diversity of bacterial endophytes in 3 and 15 year-old grapevines of Vitis vinifera cv. Corvina and their potential for plant growth promotion and phytopathogen control. Microbiol Res 183:42–52

  6. Bai SH, Dempsey R, Reverchon F, Blumfield TJ, Ryan S, Cernusak L (2017) Effects of forest thinning on soil-plant carbon and nitrogen dynamics. Plant Soil 411:437–449

  7. Bai SH, Sun F, Blumfield TJ, Xu ZH (2013) Ecophysiological status of different growth stage of understorey Acacia leiocalyx and A. disparimma in an Australian dry sclerophyll forest subjected to prescribed burning. J Soils Sediments 13:1378–1385

  8. Bai SH, Blumfield TJ, Xu ZH, Chen CR, Wild C (2012) Appraisal of 15N enrichment and 15N natural abundance methods for estimating N2 fixation by Acacia leiocalyx and A. disparimma in a native forest of subtropical Australia. J Soils Sediments 12:653–662

  9. Batterman S, Hedin L, Breugel MV, Ransijn J, Craven D, Hall J (2013) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227

  10. Birnbaum C, Bissett A, Teste FP, Laliberté E (2018) 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(4):1009–1020

  11. Brosius J, Palmer ML, Kennedy PJ, Noller HF (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A 75:4801–4805

  12. Butler OM, Rashti MR, Lewis T, Elser JJ, Chen C (2018) High-frequency fire alters soil and plant chemistry but does not lead to nitrogen-limited growth of Eucalyptus pilularis seedlings. Plant Soil 432:191–205

  13. Cardoso P, Alves A, Silveira P, Sá C, Fidalgo C, Freitas R, Figueira E (2018) Bacteria from nodules of wild legume species: phylogenetic diversity, plant growth promotion abilities and osmotolerance. Sci Total Environ 645:1094–1102

  14. Catterall CP, Piper SD, Bunn SE, Arthur JM (2001) Flora and fauna assemblages vary with local topography in a subtropical eucalypt forest. Austral Ecol 26:56–69

  15. Catterall C, Wallace C (1987) An island in suburbia: the natural and social history of Toohey forest. Institute of Applied Environmental Research. Griffith University, Brisbane

  16. Coba de la Peña T, Pueyo JJ (2012) Legumes in the reclamation of marginal soils, from cultivar and inoculant selection to transgenic approaches. Agron Sustain Dev 32:65–91

  17. Davidson EA, Reis de Carvalho CJ, Vieira IC, Figueiredo RDO, Moutinho P, Yoko Ishida F, Primo dos Santos MT, Guerrero JB, Kalif K, Tuma Sabá R (2004) Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol Appl 14:150–163

  18. Dinnage R, Simonsen AK, Barrett LG, Cardillo M, Raisbeck-Brown N, Thrall PH, Prober SM (2019) Larger plants promote a greater diversity of symbiotic nitrogen-fixing soil bacteria associated with an Australian endemic legume. J Ecol 107:977–991

  19. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

  20. Emami S, Alikhani HA, Pourbabaei AA, Etesami H, Sarmadian F, Motessharezadeh B (2019) Effect of rhizospheric and endophytic bacteria with multiple plant growth promoting traits on wheat growth. Environ Sci Pollut R 26:19804–19813

  21. Farquhar G, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

  22. Forrester DI, Bauhus J, Cowie AL (2005) Nutrient cycling in a mixed-species plantation of Eucalyptus globulus and Acacia mearnsii. Can J For Res 35:2942–2950

  23. Guinto DF, Saffigna PG, Xu ZH, House APN, Perera MCS (1999) Soil nitrogen mineralization and organic matter composition revealed by 13C NMR spectroscopy under repeated prescribed burning in eucalypt forests of south-East Queensland. Aust J Soil Res 37:123–135

  24. Guinto DF, Xu Z, House APN, Saffigna PG (2000) Assessment of N2 fixation by understorey acacias in recurrently burnt eucalypt forests of subtropical Australia using 15N isotope dilution techniques. Can J For Res 30:112–121

  25. Guinto DF, Xu ZH, House APN, Saffigna PG (2001) Soil chemical properties and forest floor nutrients under repeated prescribed burning in eucalypt forests of south-East Queensland, Australia. N Z J For Sci 31:170–187

  26. Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting Rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:96–102

  27. Hall TA (1999) BioEdit: a friendly biological sequence alignment editor and analysis program for window 95/98/NT. Nucleic Acids Symp Ser 41:95–98

  28. Hendricks JL, Boring LR (1999) N2-fixation by native herbaceous legumes in burned pine ecosystems of the southwestern United States. For Ecol Manag 113:167–177

  29. Hoque MS, Broadhurst LM, Thrall PH (2011) Genetic characterization of root-nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across south-eastern Australia. Int J Syst Evol Microbiol.61:299–309

  30. Huang W, Xu Z, Chen C, Zhou G, Liu J, Abdullah KM, Reverchon F, Liu X (2013) Short-term effects of prescribed burning on phosphorus availability in a suburban native forest of subtropical Australia. J Soils Sediments 13:869–876

  31. Isaac ME, Harmand JM, Lesueur D, Lelon J (2011) Tree age and soil phosphorus conditions influence N2-fixation rates and soil N dynamics in natural populations of Acacia senegal. For Ecol Manag 261:582–588

  32. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

  33. Ledger T, Rojas S, Timmermann T, Pinedo I, Poupin MJ, Garrido T, Richter P, Tamayo J, Donoso R (2016) Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front Microbiol 7:1838

  34. Leite J, Fischer D, Rouws LF, Fernandes-Júnior PI, Hofmann A, Kublik S, Schloter M, Xavier GR, Radl V (2017) Cowpea nodules harbor non-rhizobial bacterial communities that are shaped by soil type rather than plant genotype. Front Plant Sci 7:2064

  35. Ma L, Rao X, Lu P, Bai SH, Xu Z, Chen X, Blumfield TJ, Xie J (2015) Ecophysiological and foliar nitrogen concentration responses of understorey Acacia spp. and Eucalyptus sp. to prescribed burning. Environ Sci Pollut Res 22:10254–10262

  36. Marcondes de Andrade F, de Assis PT, Pereira Souza T, Sales Guimarães PH, Martins AD, Freitas Schwan R, Pasqual M, Dória J (2019) Beneficial effects of inoculation of growth-promoting bacteria in strawberry. Microbiol Res 223:120–128

  37. May BM, Attiwill PM (2003) Nitrogen-fixation by Acacia dealbata and changes in soil properties 5 years after mechanical disturbance or slash-burning following timber harvest. For Ecol Manag 181:339–355

  38. Méndez-Bravo A, Cortazar-Murillo EM, Guevara-Avendaño E, Ceballos-Luna O, Rodríguez-Haas B, Kiel-Martínez AL, Hernández-Cristóbal O, Guerrero-Analco JA, Reverchon F (2018) Plant growth-promoting rhizobacteria associated with avocado display antagonistic activity against Phytophthora cinnamomi through volatile emissions. PLoS One 13:e0194665

  39. Mohale KC, Belane AK, Dakora FD (2014) Symbiotic N nutrition, C assimilation, and plant water use efficiency in Bambara groundnut (Vigna subterranea L. Verdc) grown in farmers’ fields in South Africa, measured using 15N and 13C natural abundance. Biol Fertil Soils 50:307–319

  40. Muqaddas B, Lewis T, Esfandbod M, Chen C (2019) Responses of labile soil organic carbon and nitrogen pools to long-term prescribed burning regimes in a wet sclerophyll forest of Southeast Queensland, Australia. Sci Total Environ 647:110–120

  41. Muresu R, Porceddu A, Sulas L, Squartini A (2019) Nodule-associated microbiome diversity in wild populations of Sulla coronaria reveals clues on the relative importance of culturable rhizobial symbionts and co-infecting endophytes. Microbiol Res 221:10–14

  42. National Forest Inventory (2007) Australia's forests at a glance. National Forest Inventory, Bureau of Rural Sciences, Canberra

  43. Ndungu SM, Messmer MM, Ziegler D, Gamper HA, Mészáros É, Thuita M, Vanlauwe B, Frossard E, Thonar C (2018) Cowpea (Vigna unguiculata L. Walp) hosts several widespread bradyrhizobial root nodule symbionts across contrasting agro-ecological production areas in Kenya. Agric Ecosyst Environ 261:161–171

  44. Penman TD, York A (2010) Climate and recent fire history affect fuel loads in Eucalyptus forests: implications for fire management in a changing climate. For Ecol Manag 260:1791–1797

  45. Rastetter EB, Vitousek PM, Field C, Shaver GR, Herbert D (2001) Resource optimization and symbiotic nitrogen fixation. Ecosystems 4:369–388

  46. Reverchon F, Xu ZH, Blumfield TJ, Chen CR, Abdullah KM (2012) Impact of global climate change and fire on the occurrence and function of understorey legumes in forest ecosystems. J Soils Sediments 12:150–160

  47. Reverchon F, Yang H, Ho TY, Yan G, Wang J, Xu Z, Chen C, Zhang D (2015) A preliminary assessment of the potential of using an acacia—biochar system for spent mine site rehabilitation. Environ Sci Pollut Res 22:2138–2144

  48. Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey P, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

  49. Shearer G, Kohl DH (1986) N2 fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756

  50. Sprent JI (1995) Legume trees and shrubs in the tropics: N2 fixation in perspective. Soil Biol Biochem 27:401–407

  51. Sullivan BW, Nifong RL, Nasto MK, Alvarez-Clare S, Dencker CM, Soper FM, Shoemaker KT, Ishida FY, Zaragoza-Castells J, Davidson EA, Cleveland CC (2019) Biogeochemical recuperation of lowland tropical forest during succession. Ecology 100:e02641

  52. Tariq M, Hameed S, Yasmeen T, Ali A (2012) Non-rhizobial bacteria for improved nodulation and grain yield of mung bean (Vigna radiata (L.) Wilczek). Afr J Biotechnol 11(84):15012–15019

  53. Taylor BN, Chazdon RL, Menge DN (2019) Successional dynamics of nitrogen fixation and forest growth in regenerating Costa Rican rainforests. Ecology 100:e02637

  54. 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 37:52–65

  55. Tierney JA, Hedin LO, Wurzburger N (2019) Nitrogen fixation does not balance fire-induced nitrogen losses in longleaf pine savannas. Ecology 100:e02735

  56. Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochem 46:179–202

  57. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

  58. Wang Y, Xu Z, Zheng J, Abdullah KM, Zhou Q (2015) δ15N of soil nitrogen pools and their dynamics under decomposing leaf litters in a suburban native forest subject to repeated prescribed burning in Southeast Queensland, Australia. J Soils Sediments 15:1063–1074

  59. West JB, Hille Ris Lambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530

  60. Witt GB, English NB, Balanzategui D, Hua Q, Gadd P, Heijnis H, Bird MI (2017) The climate reconstruction potential of Acacia cambagei (gidgee) for semi-arid regions of Australia using stable isotopes and elemental abundances. J Arid Environ 136:19–27

  61. Xu ZH, Prasolova NV, Lundkvist K, Beadle C, Leaman T (2003) Genetic variation in branchlet carbon and nitrogen isotope composition and nutrient concentration of 11-year-old hoop pine families in relation to tree growth in subtropical Australia. For Ecol Manag 186:359–371

  62. Xu ZH, Saffigna PG, Farquhar GD, Simpson JA, Haines RJ, Walker S, Osborne DO, Guinto D (2000) Carbon isotope discrimination and oxygen isotope composition in clones of the F(1) hybrid between slash pine and Caribbean pine in relation to tree growth, water-use efficiency and foliar nutrient concentration. Tree Physiol 20:1209–1217

  63. Yang L, Liu N, Ren H, Wang J (2009) Facilitation by two exotic Acacia: Acacia auriculiformis and Acacia mangium as nurse plants in South China. For Ecol Manag 257:1786–1793

  64. Zhang B, Du N, Li Y, Shi P, Wei G (2018) Distinct biogeographic patterns of rhizobia and non-rhizobial endophytes associated with soybean nodules across China. Sci Tot Environ 643:569–578

  65. Zhao LF, Xu YJ, Ma ZQ, Deng ZS, Shan CJ, Wei GH (2013) Colonization and plant growth promoting characterization of endophytic Pseudomonas chlororaphis strain Zong1 isolated from Sophora alopecuroides root nodules. Braz J Microbiol 44:629–637

Download references

Acknowledgements

We thank Bob Coutts and Gary Bacon for their help with plant species identification; Rene Diocares, Geoffrey Lambert and Marijke Heenan for their technical support; and Alfonso Méndez for his help with image editing. We are also grateful to the Brisbane City Council for their assistance with allowing site access and fire history information.

Funding information

Funding support was from the Australian Research Council (DP0664154, DP0667184, LX0881973, DP1092470).

Author information

Correspondence to Frédérique Reverchon.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Yongfu Li

Electronic supplementary material

ESM 1

(DOCX 35.7 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Reverchon, F., Abdullah, K.M., Bai, S.H. et al. Biological nitrogen fixation by two Acacia species and associated root-nodule bacteria in a suburban Australian forest subjected to prescribed burning. J Soils Sediments 20, 122–132 (2020) doi:10.1007/s11368-019-02446-9

Download citation

Keywords

  • Nitrogen isotope composition (δ15N)
  • Rhizobia
  • Symbiotic N2 fixation
  • Understorey acacia