Abstract
Aims
Plant invasion can alter the soil microbial community and carbon cycling in terrestrial ecosystems; however, shifts in soil autotrophic bacterial communities and their driving environmental factors after plant invasion remain largely unknown. This study examined the relationship between Moso bamboo (Phyllostachys pubscens) invasion into broadleaf forests and autotrophic bacterial community composition-function at two field sites.
Methods
The abundance and composition of autotrophic bacteria were characterized by real-time PCR, terminal restriction fragment length polymorphism, and clone library based on the cbbL gene that encodes ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO).
Results
On average, the cbbL gene abundance was 89% higher and RubisCO enzyme activity 110% higher in the bamboo forest than in the broadleaf forests across the two field sites. The cbbL gene abundance was positively correlated with the RubisCO enzyme activity. The cbbL-containing communities were dominated by the order Rhizobiales, and their composition differed between the forest types and between the two sites, with the effect of site location being greater. Soil readily-oxidizable carbon concentration was a critical factor determining the site location effect on the diversity and activity of the cbbL-containing community.
Conclusion
Greater abundance and activity of autotrophic bacteria were associated with bamboo invasion into broadleaf forests, implying that such invasions are expected to increase the CO2 fixation potential.
This is a preview of subscription content, access via your institution.





References
Alfreider A, Schirmer M, Vogt C (2012) Diversity and expression of different forms of RubisCO genes in polluted groundwater under different redox conditions. FEMS Microbiol Ecol 79:649–660
Arneth A, Kelliher F, McSeveny T, Byers J (1998) Net ecosystem productivity, net primary productivity and ecosystem carbon sequestration in a Pinus radiata plantation subject to soil water deficit. Tree Physiol 18:785–793
Bai SB, Conant RT, Zhou GM, Wang YX, Wang N, Li YH, Zhang KQ (2016) Effects of moso bamboo encroachment into native, broad-leaved forests on soil carbon and nitrogen pools. Sci Rep 6:31480
Bai SB, Zhou GM, Wang YX, Liang QQ, Chen J, Cheng Y, Shen R (2013) Plant species diversity and dynamics in forests invaded by Moso bamboo (Phyllostachys edulis) in Tianmu Mountain Nature Reserve. Biodivers Sci 21:288–295 (in Chinese with an English abstract)
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20: 634–641
Bardgett RD, Richter A, Bol R, Garnett MH, Bäumler R, Xu X, Lopez-Capel E, Manning DA, Hobbs PJ, Hartley IR, Wanek W (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol Lett 3:487–490
Bardgett RD, Walker LR (2004) Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biol Biochem 36:555–559
Berg IA (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microb 77:1925–1936
Blair GJ, Lefroy RD, Lisle L (1995) Soil carbon fractions based on their degree of oxidation, and the development of a carbon management index for agricultural systems. Crop Pasture Sci 46:1459–1466
Chang EH, Chiu CY (2015) Changes in soil microbial community structure and activity in a cedar plantation invaded by moso bamboo. Appl Soil Ecol 91:1–7
Chen XG, Zhang XQ, Zhang YP, Booth T, He XH (2009) Changes of carbon stocks in bamboo stands in China during 100 years. Forest Ecol Manag 258:1489–1496
Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10:171
De’Ath G (2002) Multivariate regression trees: a new technique for modeling species-environment relationships. Ecology 83:1105–1117
Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523
Eichorst SA, Kuske CR, Schmidt TM (2011) Influence of plant polymers on the distribution and cultivation of bacteria in the phylum acidobacteria. Appl Environ Microb 77:586–596
Fukushima K, Usui N, Ogawa R, Tokuchi N (2015) Impacts of moso bamboo (Phyllostachys pubescens) invasion on dry matter and carbon and nitrogen stocks in a broad-leaved secondary forest located in Kyoto, western Japan. Plant Spec Biol 30:81–95
Gourion B, Delmotte N, Bonaldi K, Nouwen N, Vorholt JA, Giraud E (2011) Bacterial RuBisCO is required for efficient Bradyrhizobium/Aeschynomene symbiosis. PLoS One 6:e21900
Grayston SJ, Campbell CD, Bardgett RD, Mawdsley JL, Clegg CD, Ritz K, Griffiths BS, Rodwell JS, Edwards SJ, Davies WJ, Elston DJ, Millard P (2004) Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Appl Soil Ecol 25:63–84
Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296
Guo GX, Kong WD, Liu JB, Zhao JX, Du HD, Zhang XZ, Xia PH (2015) Diversity and distribution of autotrophic microbial community along environmental gradients in grassland soils on the Tibetan Plateau. Appl Microbiol Biot 99:8765–8776
Hopkins DW, Sparrow AD, Novis PM, Gregorich EG, Elberling B, Greenfield LG (2006) Controls on the distribution of productivity and organic resources in Antarctic Dry Valley soils. Proc R Soc B 273:2687–2695
Hart KM, Kulakova AN, Allen CC, Simpson AJ, Oppenheimer SF, Masoom H, Courtier-Murias D, Soong R, Kulakov LA, Flanagan PV, Murphy BT, Kelleher BP (2013) Tracking the fate of microbially sequestered carbon dioxide in soil organic matter. Environ Sci Technol 47:5128–5137
Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985
Kellermann C, Selesi D, Lee N, Hügler M, Esperschütz J, Hartmann A, Griebler C (2012) Microbial CO2 fixation potential in a tar-oil-contaminated porous aquifer. FEMS Microbiol Ecol 81:172–187
Kong WD, 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 Microb 78:4358–4366
Kusian B, Bowien B (1997) Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 21:135–155
Lacis AA, Schmidt GA, Rind D, Ruedy RA (2010) Atmospheric CO2: principal control knob governing Earth’s temperature. Science 330:356–359
Li YC, Li YF, Chang SX, Xu QF, Guo ZY, Gao Q, Qin ZY, Yang YF, Chen JH, Liang X (2017a) Bamboo invasion of broadleaf forests altered soil fungal community closely linked to changes in soil organic C chemical composition and mineral N production. Plant Soil 418:507–521
Li YC, Li YF, Chang SX, Liang X, Qin H, Chen JH, Xu QF (2017b) Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests. Soil Biol Biochem 107:19–31
Li YF, Zhang JJ, Chang SX, Jiang PK, Zhou GM, Fu SL, Yan ER, Wu JS, Lin L (2013) Long-term management effects on soil organic carbon pools and chemical composition in Moso bamboo (Phyllostachys pubescens) forests in subtropical China. Forest Ecol Manag 303:121–130
Liao CZ, Peng RH, Luo YQ, Zhou XH, Wu XW, Fang CM, Chen JK, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714
Lin YT, Tang SL, Pai CW, Whitman WB, Coleman DC, Chiu CY (2014) Changes in the soil bacterial communities in a cedar plantation invaded by moso bamboo. Microb Ecol 67:421–429
Liu J, Yang QP, Song QN, Yu DK, Yang GY, Qi HY, Shi JM (2013) Strategy of fine root expansion of Phyllostachys pubescens population into evergreen broadleaved forest. Chin J Plant Ecol 37:230–238 (in Chinese with an English abstract)
Lynn TM, Ge TD, Yuan HZ, Wei XM, Wu XH, Xiao KQ, Kumaresan D, Yu SS, Wu JS, Whiteley AS (2016) Soil carbon-fixation rates and associated bacterial diversity and abundance in three natural ecosystems. Microb Ecol (3):645–657
Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests MASS (2007) The vegan package. Community ecology package 10:631–637
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
Poll C, Marhan S, Ingwersen J, Kandeler E (2008) Dynamics of litter carbon turnover and microbial abundance in a rye detritusphere. Soil Biol Biochem 40:1306–1321
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351
Selesi D, Schmid M, Hartmann A (2005) Diversity of green-like and red-like ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes (cbbL) in differently managed agricultural soils. Appl Environ Microb 71:175–184
Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211
Sheng H, Zhou P, Zhang YZ, Kuzyakov Y, Zhou Q, Ge TD, Wang CH (2015) Loss of labile organic carbon from subsoil due to land-use changes in subtropical China. Soil Biol Biochem 88:148–157
Shively J, Devore W, Stratford L, Porter L, Medlin L, Stevens S (1986) Molecular evolution of the large subunit of ribulose-1, 5-bisphosphate carboxylase/oxygenase (RuBisCO). FEMS Microbiol Lett 37:251–257
Skjemstad JO, Swift RS, Mcgowan JA (2006) Comparison of the particulate organic carbon and permanganate oxidation methods for estimating labile soil organic carbon. Soil Res 44:255–263
Song QN, Ouyang M, Yang QP, Lu H, Yang GY, Chen FS, Shi JM (2016) Degradation of litter quality and decline of soil nitrogen mineralization after moso bamboo (Phyllostachys pubscens) expansion to neighboring broadleaved forest in subtropical China. Plant Soil 404:113–124
Stefanowicz AM, Stanek M, Nobis M, Zubek S (2016) Species-specific effects of plant invasions on activity, biomass, and composition of soil microbial communities. Biol Fert Soils 52:841–852
Sun RB, Zhang XX, Guo XS, Wang DZ, Chu HY (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18
Tabita FR (1999) Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynth Res 60:1–28
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 T R Soc B 363:2629–2640
Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, Hirayama H, Nakagawa S, Suzuki Y, Inagaki F, Horikoshi K (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl Environ Microb 71:7310–7320
Tang CX, Weligama C, Sale P (2013) Subsurface soil acidification in farming systems: its possible causes and management options. In: Xu JM, Sparks DL (eds) Molecular Environmental Soil Science. Springer Netherlands, Dordrecht
Tolli J, King GM (2005) Diversity and structure of bacterial chemolithotrophic communities in pine forest and agroecosystem soils. Appl Environ Microb 71:8411–8418
Uchida Y, Nishimura S, Akiyama H (2012) The relationship of water-soluble carbon and hot-water-soluble carbon with soil respiration in agricultural fields. Agric Ecosyst Environ 156:116–122
Wagai R, Mayer LM, Kitayama K, Knicker H (2008) Climate and parent material controls on organic matter storage in surface soils: a three-pool, density-separation approach. Geoderma 147:23–33
Wang HC, Tian GL, Chiu CY (2016) Invasion of moso bamboo into a Japanese cedar plantation affects the chemical composition and humification of soil organic matter. Sci Rep 6:32211
Watson GM, Tabita FR (1997) Microbial ribulose 1, 5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiol Lett 146:13–22
World Reference Base for Soil Resources (WRB) (2006) A framework for international classification, correlation and communication. Food and Agriculture Organization of the United Nations, Rome
Wu JS, Jiang PK, Wang ZL (2008) The effects of Phyllostachys pubescens expansion on soil fertility in National Nature Reserve of mountain tianmu. Acta Agri Univ Jiangxi 30:689–692 (in Chinese with an English abstract)
Wu XH, Ge TD, Yuan HZ, Zhou P, Chen XB, Chen S, Brookes P, Wu JS (2014) Evaluation of an optimal extraction method for measuring D-ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) in agricultural soils and its association with soil microbial CO2 assimilation. Pedobiologia 57:277–284
Xiao KQ, Bao P, Bao QL, Jia Y, Huang FY, Su JQ, Zhu YG (2014) Quantitative analyses of ribulose-1, 5-bisphosphate carboxylase/oxygenase (RubisCO) large-subunit genes (cbbL) in typical paddy soils. FEMS Microbiol Ecol 87:89–101
Xiong JB, Liu YQ, Lin XG, Zhang HY, Zeng J, Hou JZ, Yang YP, Yao TD, Knight R, Chu HY (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466
Xu JM, Tang CX, Chen ZL (2006) The role of plant residues in pH change of acid soils differing in initial pH. Soil Biol Biochem 38:709–719
Xu QF, Jiang PK, Wu JS, Zhou GM, Shen RF, Fuhrmann JJ (2015) Bamboo invasion of native broadleaf forest modified soil microbial communities and diversity. Biol Invasions 17:433–444
Yen TM, Lee JS (2011) Comparing aboveground carbon sequestration between moso bamboo (Phyllostachys heterocycla) and China fir (Cunninghamia lanceolata) forests based on the allometric model. Forest Ecol Manag 261:995–1002
Yuan HZ, Ge TD, Chen CY, O'Donnell AG, Wu JS (2012a) Significant role for microbial autotrophy in the sequestration of soil carbon. Appl Environ Microb 78:2328–2336
Yuan HZ, Ge TD, Wu XH, Liu SL, Tong CL, Qin HL, Wu M, Wei WX, Wu JS (2012b) Long-term field fertilization alters the diversity of autotrophic bacteria based on the ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large-subunit genes in paddy soil. Appl Microbiol Biot 95:1061–1071
Yuan HZ, Ge TD, Zou SY, Wu XH, Liu SL, Zhou P, Chen XJ, Brookes P, Wu JS (2013) 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 Fert Soils 49:609–616
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045
Zhou GM, Meng CF, Jiang PK, Xu QF (2011) Review of carbon fixation in bamboo forests in China. Bot Rev 77:262–270
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China (31670618, 31570602, 31470626) and the Natural Science Foundation of Zhejiang Province (No. LY15C160006). We thank Dr. Guangxia Guo and Prof. Weidong Kong at the Institute of Tibetan Plateau Research, Chinese Academy of Sciences for their assistance in RubisCO enzyme assay, and anonymous reviewers for their constructive comments that helped to improve the quality of an earlier version of this manuscript.
Author information
Affiliations
Corresponding authors
Additional information
Responsible Editor: Elizabeth M Baggs.
Electronic supplementary material
ESM 1
(DOC 67 kb)
Rights and permissions
About this article
Cite this article
Li, Y., Liang, X., Tang, C. et al. Moso bamboo invasion into broadleaf forests is associated with greater abundance and activity of soil autotrophic bacteria. Plant Soil 428, 163–177 (2018). https://doi.org/10.1007/s11104-018-3648-z
Received:
Accepted:
Published:
Issue Date:
Keywords
- Carbon cycle
- cbbL gene
- Plant invasion
- CO2-assimilating bacteria
- Ribulose-1,5-bisphosphate carboxylase/oxygenase