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Effect of land use on the abundance and diversity of autotrophic bacteria as measured by ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large subunit gene abundance in soils

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Abstract

Elucidating the biodiversity of CO2-assimilating bacterial communities under different land uses is critical for establishing an integrated view of the carbon sequestration in agricultural systems. We therefore determined the abundance and diversity of CO2 assimilating bacteria using terminal restriction fragment length polymorphism and quantitative PCR of the cbbL gene (which encodes ribulose-1,5-biphosphate carboxylase/oxygenase). These analyses used agricultural soils collected from a long-term experiment (Pantang Agroecosystem) in subtropical China. Soils under three typical land uses, i.e., rice–rice (RR), upland crop (UC), and paddy rice–upland crop rotation (PU), were selected. The abundance of bacterial cbbL (0.04 to 1.25 × 108 copies g−1 soil) and 16S rDNA genes (0.05–3.00 × 1010 copies g−1 soil) were determined in these soils. They generally followed the trend RR > PU > UC. The cbbL-containing bacterial communities were dominated by facultative autotrophic bacteria such as Mycobacterium sp., Rhodopseudomonas palustris, Bradyrhizobium japonicum, Ralstonia eutropha, and Alcaligenes eutrophus. Additionally, the cbbL-containing bacterial community composition in RR soil differed from that in upland crop and paddy rice–upland crop rotations soils. Soil organic matter was the most highly statistically significant factor which positively influenced the size of the cbbL-containing population. The RR management produced the greatest abundance and diversity of cbbL-containing bacteria. These results offer new insights into the importance of microbial autotrophic CO2 fixation in soil C cycling.

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Abbreviations

T-RFLP:

Terminal restriction fragment length polymorphism

CO2 :

Carbon dioxide

SOC:

Soil organic C

RR:

Rice–rice

UC:

Upland crop

TRF:

Terminal restriction fragment

PU:

Paddy rice–upland crop rotation

References

  • Acosta-Martíneza V, Acosta-Mercadob D, Sotomayor-Ramírezc D, Cruz-Rodríguez L (2008) Microbial communities and enzymatic activities under different management in semiarid soils. Appl Soil Ecol 38:249–260

    Article  Google Scholar 

  • Alfreider A, Vogt C, Hoffman D, Babel W (2003) Diversity of ribulose 1,5-bisphosphate carboxylase/oxygenase large subunit genes from groundwater and aquifer microorganisms. Microb Ecol 45:317–328

    Article  PubMed  CAS  Google Scholar 

  • Alfreider A, Vogt C, Geiger-Kaiser M, Psenner R (2009) Distribution and diversity of autotrophic bacteria in groundwater systems based on the analysis of RubisCO genotypes. Syst Appl Microbiol 32:140–150

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Bek EJ (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59:1525–1541

    Article  PubMed  CAS  Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499

    Article  Google Scholar 

  • Chen Z, Luo XQ, Hu RG, Wu MN, Wu JS, Wei WX (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb Ecol 60:850–861

    Article  PubMed  CAS  Google Scholar 

  • Clement BG, Kehl LE, DeBord KL, Kitts CL (1998) Terminal restriction fragment patterns (TRFPs), a rapid, PCR-based method for the comparison of complex bacterial communities. J Microbiol Meth 31:135–142

    Article  CAS  Google Scholar 

  • Das S, Bhattacharyya P, Adhya TK (2011) Impact of elevated CO2, flooding, and temperature interaction on heterotrophic nitrogen fixation in tropical rice soils. Biol Fertil Soils 47:25–30

    Article  CAS  Google Scholar 

  • Elsaied H, Naganuma T (2001) Phylogenetic diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from deep-sea microorganisms. Appl Environ Microbiol 67:1751–1765

    Article  PubMed  CAS  Google Scholar 

  • Elsaied HE, Kimura H, Naganuma T (2007) Composition of archaeal, bacterial, and eukaryal RuBisCO genotypes in three Western Pacific arc hydrothermal vent systems. Extremophiles 11:191–202

    Article  PubMed  CAS  Google Scholar 

  • Franzluebbers AJ (2010) Achieving soil organic carbon sequestration with conservation agricultural systems in the southeastern United States. Soil Sci Sco Am J 74:347–357

    Article  CAS  Google Scholar 

  • Hugendieck I, Meyer O (1991) Genes encoding ribulosebisphosphate carboxylase and phosphoribulokinase are duplicated in Pseudomonas carboxydovorans and conserved in carboxydotrophic bacteria. Arch Microbiol 157:92–96

    Article  CAS  Google Scholar 

  • Husemann M, Klintworth R, Büttcher V, Salnikow J, Weissenborn C, Bowien B (1988) Chromosomally and plasmid-encoded gene clusters for CO2 fixation (cfx) genes in Alcaligenes eutrophus. Mol Genet Genomics 214:112–120

    Article  CAS  Google Scholar 

  • IPCC (2007) Climate change 2007. Climate change impacts, adaptation and vulnerability. IPCC Working Group II. Geneva, Switzerland

  • Kaur K, Goyal S, Kapoor KK (2008) Impact of organic fertilizers with and without chemical fertilizers on soil chemical properties and the establishment of nitrogen-fixing bacteria in the rhizosphere. Microb Environ 23:313–316

    Article  Google Scholar 

  • Kent AD, Smith DJ, Benson BJ, Triplett EW (2003) Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl Environ Microbiol 69:6768–6776

    Article  PubMed  CAS  Google Scholar 

  • King GM, Weber CF (2007) Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5:107–118

    Article  PubMed  CAS  Google Scholar 

  • Kitts CL (2001) Terminal restriction fragment patterns: a tool for comparing microbial communities and assessing community dynamics. Curr Issues Intest Microbiol 2:17–25

    PubMed  CAS  Google Scholar 

  • Kong W, Ream DC, Priscu JC, Morgan-Kiss RM (2012) Diversity and expression of RubisCO genes in a perennially ice-covered Antarctic lake during the polar night transition. Appl Environ Microbiol 78:4358–4366

    Article  PubMed  CAS  Google Scholar 

  • Kusian B, Bowien B (1997) Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 21:135–155

    Article  PubMed  CAS  Google Scholar 

  • López-Gutiérrez JC, Henry S, Hallet S, Martin-Laurent F, Catroux G, Philippot L (2004) Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J Microbiol Meth 57:399–407

    Article  Google Scholar 

  • Lukow T, Dunfield PF, Liesack W (2000) Use of the T-RFLP technique to assess partial and temporal changes in the bacterial community structure with in an agricultural soil planted with transgenic and nontransgenic potato plants. FEMS Microbiol Ecol 32:241–247

    Article  CAS  Google Scholar 

  • Marsh TL, Saxman P, Cole J, Tiedje J (2000) Terminal restriction fragment length polymorphism analysis program, a web-based research tool for microbial community analysis. Appl Environ Microbiol 66:3616–3620

    Article  PubMed  CAS  Google Scholar 

  • Meyer O, Schlegel HG (1983) Biology of aerobic carbon monoxide oxidizing bacteria. Annu Rev Microbiol 37:277–310

    Article  PubMed  CAS  Google Scholar 

  • Meyer O, Frunzke K, Gadkari D, Jacobitz S, Hugendieck I, Kraut M (1990) Utilization of carbon monoxide by aerobes: recent advances. FEMS Microbiol Rev 87:253–260

    Article  CAS  Google Scholar 

  • Midgley GF, Bond WJ, Kapos V, Ravilious C, Scharlemann JPW, Woodward F (2010) Terrestrial carbon stocks and biodiversity: key knowledge gaps and some policy implications. Curr Opin Environ Sustain 2:264–270

    Article  Google Scholar 

  • Nanba K, King GM, Dunfield K (2004) Analysis of facultative lithotroph distribution and diversity on volcanic deposits by use of the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase. Appl Environ Microbiol 70:2245–2253

    Article  PubMed  CAS  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, CT Jh, Sumner ME (eds) Methods of soil analysis. Part 3—chemical methods. Soil Science Society of America, Madison, pp 961–1010

    Google Scholar 

  • Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison FR, Gebreyesus B, Lebauer D, Scow KM (2004) Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 70:1008–1016

    Article  PubMed  CAS  Google Scholar 

  • Osborn AM, Moore ERB, Timmis KN (2000) An evaluation of terminal restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2:39–50

    Article  PubMed  CAS  Google Scholar 

  • Paul J, Alfreider A, Wawrik B (2000) Micro and macro diversity in rbcL sequences in ambient phytoplankton populations from the southeastern Gulf of Mexico. Mar Ecol Prog Ser 198:9–18

    Article  CAS  Google Scholar 

  • Salles JF, Van Veen JA, Van Elsas JD (2004) Multivariate analyses of Burkholderia species in soil: effect of crop and land use history. Appl Environ Microbiol 70:4012–4020

    Article  PubMed  CAS  Google Scholar 

  • Selesi D, Schmid M, Hartmann A (2005) Diversity of green-like and red-like ribulose 1.5-bisphosphatecarboxylase/oxygenase large-subunit genes (cbbL) in differently managed agricultural soils. Appl Environ Microbiol l71:175–184

    Article  Google Scholar 

  • Selesi D, Pattis I, Schmid M, Kandeler E, Hartmann A (2007) Quantification of bacterial RubisCO genes in soils by cbbL targeted real-time PCR. J Microbiol Methods 69:497–503

    Article  PubMed  CAS  Google Scholar 

  • Shannon CE (2001) A mathematical theory of communication. ACM SIGMOBILE Mob Comp Comm Rev 5(1):3–55

    Article  Google Scholar 

  • Shively JM, English RS, Baker SH, Cannon GC (2001) Carbon cycling: the prokaryotic contribution. Curr Opin Microbiol 4:301–306

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sombrero A, de Benitoa A (2010) Carbon accumulation in soil. Ten-year study of conservation tillage and crop rotation in a semi-arid area of Castile-Leon, Spain. Soil Tillage Res 107:64–70

    Article  Google Scholar 

  • Tabita FR (1999) Microbial ribulose-1,5-bisphosphatecarboxylase/oxygenase: a different perspective. Photosynth Rev 60:1–28

    Article  CAS  Google Scholar 

  • Tabita FR, Hanson TE, Satagopan S, Witte BH, Kreel NE (2008) Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Philos Trans R Soc Lond B Biol Sci 363:2629–2640

    Article  PubMed  CAS  Google Scholar 

  • Tolli J, King GM (2005) Diversity and structure of bacterial chemolithotrophic communities in pine forest and agroecosystem soils. Appl Environ Microbiol 71:8411–8418

    Article  PubMed  CAS  Google Scholar 

  • Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    Article  PubMed  CAS  Google Scholar 

  • Turova TP, Spiridonova EM (2009) Phylogeny and evolution of the ribulose 1,5-bisphosphate carboxylase/oxygenase genes in prokaryotes. Mol Biol 43:713–728

    Article  Google Scholar 

  • van der Wielen PWJJ (2006) Diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes in the MgCl2-dominated deep hypersaline anoxic basin discovery. FEMS Microbiol Lett 259:326–331

    Article  PubMed  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) Microbial biomass measurements in forest soils: determination of kc values and tests of hypotheses to explain the failure of the chloroform fumigation–incubation method in acid soils. Soil Biol Biochem 19:689–696

    Article  Google Scholar 

  • Videmšek U, Hagn A, Suhadolc M, Radl V, Knicker H, Schloter M, Vodnik D (2009) Abundance and diversity of CO2-fixing bacteria in grassland soils close to natural carbon dioxide springs. Microb Ecol 58:1–9

    Article  PubMed  Google Scholar 

  • Witte B, John D, Wawrik B, Paul JH, Dayan D, Tabita F (2010) Functional prokaryotic RubisCO from an oceanic metagenomic library. Appl Environ Microbiol 76:2997–3003

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation–extraction—an automated procedure. Soil Biol Biochem 22:1167–1169

    Article  CAS  Google Scholar 

  • Xu HH, Tabita FR (1996) Ribulose-1,5-bisphosphatecarboxylase/oxygenasegene expression and diversity of Lake Erie planktonic microorganisms. Appl Environ Microbiol 62:1913–1921

    PubMed  CAS  Google Scholar 

  • Yao H, He Z, Wilson MJ, Campbell CD (2000) Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microb Ecol 40:223–237

    PubMed  CAS  Google Scholar 

  • Yousuf B, Sanadhya P, Keshri J, Jha B (2012) Comparative molecular analysis of chemolithoautotrophic bacterial diversity and community structure from coastal saline soils, Gujarat, India. BMC Microbiol 12:150–164

    Article  PubMed  CAS  Google Scholar 

  • Yuan HZ, Ge TD, Chen CY, O’Donnell AG, Wu JS (2012a) Microbial autotrophy plays a significant role in the sequestration of soil carbon. Appl Environ Microbiol 78:2328–2336

    Article  PubMed  CAS  Google Scholar 

  • Yuan HZ, Ge TD, Wu XH, Liu SL, Tong CL, Qin HL, Wu MN, Wei WX, Wu JS (2012b) Long-term field fertilization alters the div ersity of autotrophic bacteria based on the ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large-subunit genes in paddy soil. Appl Microbiol Biotechnol 95:1061–1071

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the “Strategic Priority Research Program—Climate Change: Carbon Budget and Related Issues” of the Chinese Academy of Sciences (XDA05050505), National Natural Science Foundation of China (41090283; 41271279), the CAS/SAFEA International Partnership Program for Creative Research Teams (KZCX2-YW-T07; 20100491005-8) and the Knowledge Innovation Program of the Chinese Academy of Sciences (ISACX-LYQY-QN-1103).

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Correspondence to Jinshui Wu.

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Yuan, H., Ge, T., Zou, S. et al. Effect of land use on the abundance and diversity of autotrophic bacteria as measured by ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large subunit gene abundance in soils. Biol Fertil Soils 49, 609–616 (2013). https://doi.org/10.1007/s00374-012-0750-x

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