Biodiversity, abundance, and activity of nitrogen-fixing bacteria during primary succession on a copper mine tailings
Li-Nan Huang
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorFeng-Zao Tang
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorYong-Sheng Song
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorCai-Yun Wan
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorSheng-Long Wang
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorWei-Qiu Liu
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Wen-Sheng Shu
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Correspondence: Wen-Sheng Shu, School of Life Sciences, Sun Yat-Sen University, Xingang West Road 135, Guangzhou 510275, China. Tel.: +86 20 39332933; fax: +86 20 39332944; e-mail: [email protected]Search for more papers by this authorLi-Nan Huang
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorFeng-Zao Tang
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorYong-Sheng Song
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorCai-Yun Wan
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorSheng-Long Wang
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorWei-Qiu Liu
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Wen-Sheng Shu
School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, China
Correspondence: Wen-Sheng Shu, School of Life Sciences, Sun Yat-Sen University, Xingang West Road 135, Guangzhou 510275, China. Tel.: +86 20 39332933; fax: +86 20 39332944; e-mail: [email protected]Search for more papers by this authorAbstract
Microorganisms are important in soil development, inputs and biogeochemical cycling of nutrients and organic matter during early stages of ecosystem development, but little is known about their diversity, distribution, and function in relation to the chemical and physical changes associated with the progress of succession. In this study, we characterized the community structure and activity of nitrogen-fixing microbes during primary succession on a copper tailings. Terminal fragment length polymorphism (T-RFLP) and clone sequencing of nifH genes indicated that different N2-fixing communities developed under primary succession. Phylogenetic analysis revealed a diversity of nifH sequences that were mostly novel, and many of these could be assigned to the taxonomic divisions Proteobacteria, Cyanobacteria, and Firmicutes. Members of the Cyanobacteria, mostly affiliated with Nostocales or not closely related to any known organisms, were detected exclusively in the biological soil crusts and represented a substantial fraction of the respective diazotrophic communities. Quantitative PCR (and statistical analyses) revealed that, overall, copy number of nifH sequences increased with progressing succession and correlated with changes in physiochemical properties (including elementary elements such as carbon and nitrogen) and the recorded nitrogenase activities of the tailings. Our study provides an initial insight into the biodiversity and community structure evolution of N2-fixing microorganisms in ecological succession of mine tailings.
References
- Bormann BT & Sidle RC (1990) Changes in productivity and distribution of nutrients in a chronosequence at Glacier Bay National Park, Alaska. J Ecol 78: 561–578.
- Buckley DH, Huangyutitham V, Hsu SF & Nelson TA (2007) Stable isotope probing with 15N2 reveals novel noncultivated diazotrophs in soil. Appl Environ Microbiol 73: 3196–3204.
- Chapin FS, Walker LR, Fastie CL & Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64: 149–175.
- Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310.
- Deiglmayr K, Philippot L, Tscherko D & Kandeler E (2006) Microbial succession of nitrate-reducing bacteria in the rhizosphere of Poa alpina across a glacier foreland in the Central Alps. Environ Microbiol 8: 1600–1612.
- Dobson AP, Bradshaw AD & Baker AJ (1997) Hopes for the future: restoration ecology and conservation biology. Science 277: 515–522.
- Duc L, Noll M, Meier BE, Bürgmann H & Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding alpine glacier. Microb Ecol 57: 179–190.
- Edwards IP, Bürgmann H, Miniaci C & Zeyer J (2006) Variation in microbial community composition and culturability in the rhizosphere of Leucanthemopsis alpina (L.) Heywood and adjacent bare soil along an alpine chronosequence. Microb Ecol 52: 679–692.
- Frostegård A & Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22: 59–65.
- Good IJ (1953) The population frequencies of species and estimation of population parameters. Biometrika 40: 237–264.
- Hardy RWF & Holsten RD (1977) Methods for measurement of dinitrogen fixation. A Treatise of Dinitrogen Fixation. Section 4: Agronomy and Ecology ( RWF Hardy & AH Gibson, eds), pp. 451–486. John Wiley & Sons Inc., New York, NY.
- Héry M, Philippot L, Mériaux E, Poly F, Le Roux X & Navarro E (2005) Nickel mine spoils revegetation attempts: effect of pioneer plants on two functional bacterial communities involved in the N-cycle. Environ Microbiol 7: 486–498.
- Ibekwe AM & Kennedy AC (1998) Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and greenhouse conditions. FEMS Microbiol Ecol 26: 151–163.
- Jumpponen A (2003) Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses. New Phytol 158: 569–578.
10.1046/j.1469-8137.2003.00767.x Google Scholar
- Kandeler E, Deiglmayr K, Tscherko D, Bru D & Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72: 5957–5962.
- Lazzaro A, Abegg C & Zeyer J (2009) Bacterial community structure of glacier forefields on siliceous and calcareous bedrock. Eur J Soil Sci 60: 860–870.
- Ledin M & Pedersen K (1996) The environmental impact of mine wastes – roles of microorganisms and their significance in treatment of mine wastes. Earth-Sci Rev 41: 67–108.
- MacNaughton SJ, Stephen SR, Venosa AD, Davis GD, Chang YJ & White DC (1999) Microbial population changes during bioremediation of an experimental oil spill. Appl Environ Microbiol 65: 3566–3574.
- Marilley L & Aragno M (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13: 127–136.
- Marrs RH & Bradshaw AD (1993) Primary succession on manmade wastes: the importance of resource acquisition. Primary Succession on Land ( J Miles & DWH Walton, eds), pp. 113–136. Blackwell, Oxford, UK.
- Matthews JA (1992) The Ecology of Recently-Deglaciated Terrain: A Geoecological Approach to Glacier Forelands and Primary Succession. Cambridge University Press, Cambridge, UK.
- Mendez MO & Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments–an emerging remediation technology. Environ Health Perspect 116: 278–283.
- Mendez MO, Neilson JW & Maier RM (2008) Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailing site. Appl Environ Microbiol 74: 3899–3907.
- Merilä P, Galand PE, Fritze H, Tuittila ES, Kukko-Oja K, Laine J & Yrjälä K (2006) Methanogen communities along a primary succession transect of mire ecosystems. FEMS Microbiol Ecol 55: 221–229.
- Moynahan OS, Zabinski CA & Gannon JE (2002) Microbial community structure and carbon-utilization diversity in a mine tailings revegetation study. Restor Ecol 10: 77–87.
- Nicol GW, Tscherko D, Embley TM & Prosser JI (2005) Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ Microbiol 7: 337–347.
- Ohtonen R, Fritze H, Pennanen T, Jumpponen A & Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119: 239–246.
- Page AC, Miller RH & Keeney DR (1982) Methods of Soil Analyses. Part 2. Chemical and Microbiological Properties. American Society of Agronomy, Madison, WI.
- Patriquin DG & Denike D (1978) In situ acetylene-reduction assay of nitrogenase activity associated with the emergent halophyte Spartina alterniflora Loisel: methodological problems. Aquat Bot 4: 211–226.
- Petersen SO & Klug MJ (1994) Effects of sieving, storage, and incubation temperature on the phospholipid fatty acid profiles of a soil microbial community. Appl Environ Microbiol 60: 2421–2430.
- Poly F, Ranjard L, Nazaret S, Gourbière F & Monrozier LJ (2001) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67: 2255–2262.
- Redfield E, Barns SM, Belnap J, Daane LL & Kuske CR (2002) Comparative diversity and composition of cyanobacteria in three predominant soil crusts of the Colorado Plateau. FEMS Microbiol Ecol 40: 55–63.
- Schipper LA, Degens BP, Sparling GP & Duncan LC (2001) Changes in microbial heterotrophic diversity along five plant successional sequences. Soil Biol Biochem 33: 2093–2103.
- Schloss PD & Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501–1506.
- Schmidt SK, Reed SC, Nemergut DR et al. (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc Biol Sci 275: 2793–2802.
- Schütte UM, Abdo Z, Bent SJ, Williams CJ, Schneider GM, Solheim B & Forney LJ (2009) Bacterial succession in a glacier foreland of the High Arctic. ISME J 3: 1258–1268.
- Shu WS, Ye ZH, Zhang ZQ, Lan CY & Wong MH (2005) Natural colonization of plants on five lead/zinc mine tailings in southern China. Restor Ecol 13: 49–60.
- Singleton DR, Furlong MA, Rathbun SL & Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67: 4374–4376.
- Sun QY, An SQ, Yang LZ & Wang ZS (2004) Chemical properties of the upper tailings beneath biotic crusts. Ecol Eng 23: 47–53.
- Tscherko D, Hammesfahr U, Marx MC & Kandeler E (2004) Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36: 1685–1698.
- Turicchia S, Ventura S, Schutte UME, Soldati E, Zielke M & Solheim B (2005) Biodiversity of the cyanobacterial community in the foreland of the retreating glacier Midre Lovenbreen, Spitsbergen, Svalbard. Arch Hydrobiol Suppl 117: 427–440.
10.1127/1864-1318/2005/0117-0427 Google Scholar
- Walker LR & del Moral R (2003) Primary Succession and Ecosystem Rehabilitation. Cambridge University Press, Cambridge, UK.
10.1017/CBO9780511615078 Google Scholar
- Widmer F, Shaffer BT, Porteous LA & Seidler RJ (1999) Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in the Oregon cascade mountain range. Appl Environ Microbiol 65: 374–380.
- Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J & Kuske CR (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appl Environ Microbiol 70: 973–983.
- Zhang Y, Li D, Wang H, Xiao Q & Liu X (2006) Molecular diversity of nitrogen-fixing bacteria from the Tibetan Plateau, China. FEMS Microbiol Lett 260: 134–142.