Abstract
Ninety isolates of root nodule bacteria from an invasive Mimosa pigra population in Australia were characterized by PCR assays and by sequencing of ribosomal genes. All isolates belonged to the same bacterial genus (Burkholderia) that predominates on M. pigra in its native geographic range in tropical America. However, the Australian Burkholderia strains represented several divergent lineages, none of which had a close relationship to currently known Burkholderia strains in American M. pigra populations. Inoculation of M. pigra with Australian strains resulted in equal or higher plant growth and nodule nitrogenase activity (measured by acetylene reduction assays) relative to outcomes with bacteria from M. pigra’s native geographic region. The main difference in symbiotic phenotype for bacteria from the two regions involved responses to an alternate Mimosa host species: Central American strains failed to fix nitrogen in association with Mimosa pudica, while most Australian Burkholderia isolates tested had high nodule nitrogenase activity in association with both Mimosa species. Invasive M. pigra populations in Australia have therefore acquired a diverse assemblage of nodule bacteria that are effective nitrogen-fixing symbionts, despite having a broader host range and a distant genetic relationship to bacterial strains found in the plant’s ancestral region.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barneby RC (1991). Sensitive Censitae: A Description of the Genus Mimosa Linnaeus (Mimosaceae) in the New World. The New York Botanical Garden, New York, 430–439
Barrett CF and Parker MA (2005). Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama. Systematic and Applied Microbiology 28: 57–65
Barrett CF and Parker MA (2006) Coexistence of Burkholderia, Cupriavidus and Rhizobium sp. nodule bacteria on two Mimosa species in Costa Rica. Applied and Environmental Microbiology 72: 1198–1206
Bever JD (2002). Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proceedings of the Royal Society of London B 269: 2595–2601
Braithwaite RW, Lonsdale WM and Estbergs JA (1989). Alien vegetation and native biota in tropical Australia: the spread and impact of Mimosa pigra. Biological Conservation 48: 189–210
Callaway RM, Hierro JL and Thorpe AS (2005). Evolutionary trajectories in plant and soil microbial communities: Centaurea invasions and the geographic mosaic of coevolution. In: Sax, DF, Stachowicz, JJ, and Gaines, SD (eds) Species Invasions: Insights into Ecology, Evolution and Biogeography, pp 341–363. Sinauer, Sunderland, MA
Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G and Boivin-Masson C (2003). Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. Journal of Bacteriology 185: 7266–7272
Chen WM, de Faria SM, Straliotto R, Pitard RM, Simões-Araùjo JL, Chou JH, Chou YJ, Barrios E, Prescott AR, Elliot GN, Sprent JI, Young JPW and James EK (2005a). Proof that Burkholderia forms effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Applied and Environmental Microbiology 71: 7461–7471
Chen WM, James EK, Chou JH, Sheu SY, Yang SZ and Sprent JI (2005b). Beta-rhizobia from Mimosa pigra, a newly-discovered invasive plant in Taiwan. New Phytologist 168: 661–675
Clark MA, Moran NA and Baumann P (1999). Sequence evolution in bacterial endosymbionts having extreme base pair composition. Molecular Biology and Evolution 16: 1586–1598
Coenye T, Henry D, Speert DP and Vandamme P (2004). Burkholderia phenoliruptrix sp. nov., to accommodate the 2,4,5-trichlorophenoxyacetic acid and halopehnol-degrading strain AC1100. Systematic and Applied Microbiology 27: 623–627
Croat TB (1978). Flora of Barro Colorado Island. Stanford University Press, Stanford, CA, 423–485
Cronk QCB and Fuller JL (1995) Plant Invaders. Chapman & Hall, London, 241 pp
Crooks J and Soule ME (1996). Lag times in population explosions of invasive species: causes and implications. In: Sandlund, OT, Schei, PJ and Viken, A (eds) Proceedings of the Norway/UN Conference on Alien Species, pp. Directorate for Nature Management and Norweigian Insitute for Nature research, Trondhein, Norway
Davidson BR and Davidson HF (1993). Legumes: The Australian Experience – the Botany, Ecology and Agriculture of Indigenous and Immigrant Legumes. Research Studies Press Ltd., Somerset, UK, 384–407
Felsenstein J (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791
Hnatiuk RJ (1990) Census of Australian Vascular Plants. Australian Flora and Fauna Series 11. Australian Government Publishing Service Press, Canberra, 650 pp
Hobbs RJ and Humphries SE (1995). An integrated approach to the ecology and management of plant invasions. Conservation Biology 9: 761–770
Holm L, Pancho JV, Herberger JP and Plucknett DL (1979) A Geographical Atlas of World Weeds. John Wiley & Sons, New York, 391 pp
Hughes CE and Styles BT (1989). Benefits and risks of woody legume introductions. In: Stirton, CH and Zarucchi, JL (eds) Advances in Legume Biology, Monographs in Systematic Botany, 29, pp 505–531. Missouri Botanical Garden Press, St. Louis
Janzen DH (1983). Mimosa pigra (Zarza, Dormilona). In: Janzen, DH (eds) Costa Rican Natural History, pp 277–278. University of Chicago Press, Chicago
Kang H, Hwang SY, Kim YM, Kim E, Kim YS, Kim SK, Kim SW, Cerniglia CE, Shuttleworth KL and Zylstra GJ (2003). Degradation of phenanthrene and naphthalene by a Burkholderia species strain. Canadian Journal of Microbiology 49: 139–144
Kellogg ST, Chatterjee DK and Chakrabarty AM (1981). Plasmid-assisted molecular breeding: new technique for enhanced biodegradation of persistent toxic chemicals. Science 214: 1133–1135
Kilbane JJ, Chatterjee DK, Karns JS, Kellogg ST and Chakrabarty AM (1982). Biodegradation of 2,4,5-trichlorophenoxyacetic acid by a pure culture of Pseudomonas cepacia. Applied and Environmental Microbiology 44: 72–78
Klironomos JN (2002). Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67–70
Lafay B and Burdon JJ (1998). Molecular diversity of rhizobia occurring on native shrubby legumes in Southeastern Australia. Applied and Environmental Microbiology 64: 3989–3997
Lafay B and Burdon JJ (2001). Small-subunit rRNA genotyping of rhizobia nodulating Australian Acacia spp. Applied and Environmental Microbiology 67: 396–402
Lonsdale WM (1993). Rates of spread of an invading species: Mimosa pigra in northern Australia. Journal of Ecology 81: 513–521
Lonsdale WM (1994). Inviting trouble: introduced pasture species of Northern Australia. Australian Journal of Ecology 19: 345–354
Lonsdale WM and Abrecht DG (1988). Seedling mortality in Mimosa pigra, an invasive tropical shrub. Journal of Ecology 77: 371–385
Lonsdale WM, Miller IL and Forno IW (1995). Mimosa pigra L. In: Groves, RH, Shepherd, RCH, and Richardson, RG (eds) The Biology of Australian Weeds, pp 169–188. RG and FJ Richardson, Melbourne
Marsudi NDS, Glenn AR and Dilworth MJ (1999). Identification and characterization of fast- and slow-growing root nodule bacteria from South-Western Australian soils able to nodulate Acacia saligna. Soil Biology and Biochemistry 31: 1229–1238
Miller I (2005) A History of the Weed Management Branch in the Northern Territory. On: Dept. of Infrastructure Planning and Environment, Northern Territory, Australia (website). Retrieved from http://www.ipe.nt.gov.au/whatwedo/weeds/pdf/history.pdf on 4 August 2005
Moulin L, Munive A, Dreyfus B and Boivin-Masson C (2001). Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411: 948–950
Parker MA (2001). Mutualism as a constraint on invasion success for legumes and rhizobia. Diversity and Distributions 7: 125–136
Parker MA and Lunk A (2000). Relationships of bradyrhizobia from Platypodium and Machaerium (Papilionoideae tribe Dalbergieae) on Barro Colorado Island, Panama. International Journal of Systematic and Evolutionary Microbiology 50: 1179–1186
Parker MA, Lafay B and Burdon JJ (2002). Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium. Microbiology 148: 2557–2565
Paynter Q, Csurhes SM, Heard TA, Ireson J, Julien MH, Lloyd J, Lonsdale WM, Palmer WA, Sheppard AW and Van Klinken RD (2003). Worth the risk? Introduction of legumes can cause more harm than good: an Australian perspective. Australian Journal of Systematic Botany 16: 81–88
Perez-Fernandez MA and Lamont BB (2003). Nodulation and performance of exotic and native legumes in Australian soils. Australian Journal of Botany 51: 543–553
Qian J, Kwon SW and Parker MA (2003). rRNA and nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiology Letters 219: 159–165
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ and Rejmánek M (2000). Plant invasions – the role of mutualism. Biological Reviews 75: 65–93
Spoerke JM, Wilkinson HH and Parker MA (1996). Nonrandom genotypic associations in a legume-Bradyrhizobium mutualism. Evolution 50: 146–154
Sterner JP and Parker MA (1999). Diversity and relationships of bradyrhizobia from Amphicarpaea bracteata based on partial nod and ribosomal sequences. Systematic and Applied Microbiology 22: 387–392
Thompson JD, Higgins DG and 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 Research 22: 4673–4680
Turner GL and Gibson AH (1980). Measurement of nitrogen fixation by indirect means. In: Bergersen, FJ (eds) Methods for Evaluating Biological Nitrogen Fixation, pp 111–138. Wiley, New York
Vandamme P, Goris J, Chen WM, de Vos P and Willems A (2002). Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Systematic and Applied Microbiology 25: 507–512
Weir BS, Turner SJ, Silvester WB, Park DC and Young JM (2004). Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introducted legume weeds are nodulated by Bradyrhizobium species. Applied and Environmental Microbiology 70: 5980–5987
Wilkinson HH, Spoerke JM and Parker MA (1996). Divergence in symbiotic compatibility in a legume-Bradyrhizobium mutualism. Evolution 50: 1470–1477
Acknowledgements
We are grateful to J. Pfeil for assistance with sequencing, to G. Orzechowski and M. Arabov for help with PCR, and to David Sutton for providing Mimosa pigra seeds. We also thank Euan James for sharing unpublished sequence data and manuscript pre-prints. Financial support was provided by NSF grant DEB-0235766.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Parker, M.A., Wurtz, A.K. & Paynter, Q. Nodule Symbiosis of Invasive Mimosa pigra in Australia and in Ancestral Habitats: A Comparative Analysis. Biol Invasions 9, 127–138 (2007). https://doi.org/10.1007/s10530-006-0009-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-006-0009-2