Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Soil microbial responses to labile carbon input differ in adjacent sugarcane and forest soils

Richard Brackin A C , Nicole Robinson A , Prakash Lakshmanan B and Susanne Schmidt A
+ Author Affiliations
- Author Affiliations

A School of Agriculture and Food Science, The University of Queensland, St Lucia, Qld 4072, Australia.

B Sugar Research Australia, 50 Meiers Road, Indooroopilly, Qld 4068, Australia.

C Corresponding author. Email: richard.brackin@uqconnect.edu.au

Soil Research 52(3) 307-316 https://doi.org/10.1071/SR13276
Submitted: 23 September 2013  Accepted: 5 December 2013   Published: 31 March 2014

Abstract

Soil microbial activity can be constrained by availability of energy because soil carbon (C) occurs mostly as complex soil organic matter (SOM), with relatively small quantities of high-energy, labile C. Decomposition of SOM is mediated by energy-requiring processes that need extracellular enzymes produced by soil microbial communities. We examined how an increase in energy status via sucrose supplementation affects the production of SOM-degrading enzymes, comparing matched soils under forest and sugarcane agriculture with histories of contrasting inputs of complex and labile C. Activities of SOM-degrading enzymes increased in both soils after sucrose addition, but CO2 production increased more rapidly in the sugarcane soil. The forest soil had greater increases in phosphatase and glucosidase activities, whereas the sugarcane soil had greater increases in protease and urease activity. The contrasting microbial community-level physiological profiles of the soils further diverged at 30 and 61 days after sucrose amendment, before returning to near pre-treatment profiles by 150 days. We interpreted the increasing soil enzyme production as indicative that enzyme production was limited by energy availability in both soils, despite contrasting histories of labile v. recalcitrant C supply. Quicker responses in sugarcane soil suggest pre-selection towards populations that exploit labile inputs.

Additional keywords: land use change, nitrification, nitrogen, soil function.


References

Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biology & Biochemistry 33, 943–951.
Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils.Crossref | GoogleScholarGoogle Scholar |

Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology & Biochemistry 37, 937–944.
Responses of extracellular enzymes to simple and complex nutrient inputs.Crossref | GoogleScholarGoogle Scholar |

Aumtong S, de Neergaard A, Magid J (2011) Formation and remobilisation of soil microbial residue. Effect of clay content and repeated additions of cellulose and sucrose. Biology and Fertility of Soils 47, 863–874.
Formation and remobilisation of soil microbial residue. Effect of clay content and repeated additions of cellulose and sucrose.Crossref | GoogleScholarGoogle Scholar |

Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. The ISME Journal 2, 805–814.
Microbial contributions to climate change through carbon cycle feedbacks.Crossref | GoogleScholarGoogle Scholar | 18615117PubMed |

Bardgett RD, Manning P, Morrien E, De Vries FT (2013) Hierarchical responses of plant–soil interactions to climate change: consequences for the global carbon cycle. Journal of Ecology 101, 334–343.
Hierarchical responses of plant–soil interactions to climate change: consequences for the global carbon cycle.Crossref | GoogleScholarGoogle Scholar |

Bengtson P, Bengtsson G (2005) Bacterial immobilization and remineralization of N at different growth rates and N concentrations. FEMS Microbiology Ecology 54, 13–19.
Bacterial immobilization and remineralization of N at different growth rates and N concentrations.Crossref | GoogleScholarGoogle Scholar | 16329968PubMed |

Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biology and Fertility of Soils 45, 115–131.
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review.Crossref | GoogleScholarGoogle Scholar |

Blagodatskaya E, Yuyukina T, Blagodatsky S, Kuzyakov Y (2011) Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects. Soil Biology & Biochemistry 43, 778–786.
Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects.Crossref | GoogleScholarGoogle Scholar |

Boyer JN, Groffman P (1996) Bioavailability of water extractable organic carbon fractions in forest and agricultural soil profiles. Soil Biology & Biochemistry 28, 783–790.
Bioavailability of water extractable organic carbon fractions in forest and agricultural soil profiles.Crossref | GoogleScholarGoogle Scholar |

Brackin R, Robinson N, Lakshmanan P, Schmidt S (2013) Microbial function in adjacent subtropical forest and agricultural soil. Soil Biology & Biochemistry 57, 68–77.
Microbial function in adjacent subtropical forest and agricultural soil.Crossref | GoogleScholarGoogle Scholar |

Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Applied and Environmental Microbiology 69, 3593–3599.
A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil.Crossref | GoogleScholarGoogle Scholar | 12788767PubMed |

Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proceedings of the National Academy of Sciences of the United States of America 104, 4990–4995.
Altered soil microbial community at elevated CO2 leads to loss of soil carbon.Crossref | GoogleScholarGoogle Scholar | 17360374PubMed |

Chabbi A, Rumpel C (2009) Organic matter dynamics in agro-ecosystems—the knowledge gaps. European Journal of Soil Science 60, 153–157.
Organic matter dynamics in agro-ecosystems—the knowledge gaps.Crossref | GoogleScholarGoogle Scholar |

Chantigny MH (2003) Dissolved and water-extractable organic matter in soils: a review on the influence of land use and management practices. Geoderma 113, 357–380.
Dissolved and water-extractable organic matter in soils: a review on the influence of land use and management practices.Crossref | GoogleScholarGoogle Scholar |

Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Global Change Biology 19, 988–995.
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?Crossref | GoogleScholarGoogle Scholar | 23504877PubMed |

Creamer RE, Bellamy P, Black HIJ, Cameron CM, Campbell CD, Chamberlain P, Harris J, Parekh N, Pawlett M, Poskitt J, Stone D, Ritz K (2009) An inter-laboratory comparison of multi-enzyme and multiple substrate-induced respiration assays to assess method consistency in soil monitoring. Biology and Fertility of Soils 45, 623–633.
An inter-laboratory comparison of multi-enzyme and multiple substrate-induced respiration assays to assess method consistency in soil monitoring.Crossref | GoogleScholarGoogle Scholar |

Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245, 35–47.
Root exudates as mediators of mineral acquisition in low-nutrient environments.Crossref | GoogleScholarGoogle Scholar |

Dalmonech D, Lagomarsino A, Moscatelli MC, Chiti T, Valentini R (2010) Microbial performance under increasing nitrogen availability in a Mediterranean forest soil. Soil Biology & Biochemistry 42, 1596–1606.
Microbial performance under increasing nitrogen availability in a Mediterranean forest soil.Crossref | GoogleScholarGoogle Scholar |

Engelking B, Flessa H, Joergensen RG (2007) Microbial use of maize cellulose and sugarcane sucrose monitored by changes in the 13C/12C ratio. Soil Biology & Biochemistry 39, 1888–1896.
Microbial use of maize cellulose and sugarcane sucrose monitored by changes in the 13C/12C ratio.Crossref | GoogleScholarGoogle Scholar |

Engelking B, Flessa H, Joergensen RG (2008) Formation and use of microbial residues after adding sugarcane sucrose to a heated soil devoid of soil organic matter. Soil Biology & Biochemistry 40, 97–105.
Formation and use of microbial residues after adding sugarcane sucrose to a heated soil devoid of soil organic matter.Crossref | GoogleScholarGoogle Scholar |

Floch C, Alarcon-Gutierrez E, Criquet S (2007) ABTS assay of phenol oxidase activity in soil. Journal of Microbiological Methods 71, 319–324.
ABTS assay of phenol oxidase activity in soil.Crossref | GoogleScholarGoogle Scholar | 18006094PubMed |

Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biology & Biochemistry 35, 837–843.
The priming effect of organic matter: a question of microbial competition?Crossref | GoogleScholarGoogle Scholar |

Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecology Letters 7, 314–320.
Carbon input to soil may decrease soil carbon content.Crossref | GoogleScholarGoogle Scholar |

Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biology & Biochemistry 43, 86–96.
Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect.Crossref | GoogleScholarGoogle Scholar |

Gärdenäs AI, Ågren GI, Bird JA, Clarholm M, Hallin S, Ineson P, Kätterer T, Knicker H, Nilsson SI, Näsholm T, Ogle S, Paustian K, Persson T, Stendahl J (2011) Knowledge gaps in soil carbon and nitrogen interactions—From molecular to global scale. Soil Biology & Biochemistry 43, 702–717.
Knowledge gaps in soil carbon and nitrogen interactions—From molecular to global scale.Crossref | GoogleScholarGoogle Scholar |

Henderson SL, Dandie CE, Patten CL, Zebarth BJ, Burton DL, Trevors JT, Goyer C (2010) Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Applied and Environmental Microbiology 76, 2155–2164.
Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues.Crossref | GoogleScholarGoogle Scholar | 20154105PubMed |

Hernández D, Hobbie S (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant and Soil 335, 397–411.
The effects of substrate composition, quantity, and diversity on microbial activity.Crossref | GoogleScholarGoogle Scholar |

Holst J, Brackin R, Robinson N, Lakshmanan P, Schmidt S (2012) Soluble inorganic and organic nitrogen in two Australian soils under sugarcane cultivation. Agriculture, Ecosystems & Environment 155, 16–26.
Soluble inorganic and organic nitrogen in two Australian soils under sugarcane cultivation.Crossref | GoogleScholarGoogle Scholar |

Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. Journal of Plant Nutrition and Soil Science 165, 397–407.
Plant rhizodeposition—an important source for carbon turnover in soils.Crossref | GoogleScholarGoogle Scholar |

Inselsbacher E, Ripka K, Klaubauf S, Fedosoyenko D, Hackl E, Gorfer M, Hood-Novotny R, Von Wirén N, Sessitsch A, Zechmeister-Boltenstern S, Wanek W, Strauss J (2009) A cost-effective high-throughput microcosm system for studying nitrogen dynamics at the plant-microbe-soil interface. Plant and Soil 317, 293–307.
A cost-effective high-throughput microcosm system for studying nitrogen dynamics at the plant-microbe-soil interface.Crossref | GoogleScholarGoogle Scholar |

Isbell RF (2002) ‘The Australian Soil Classification.’ Revised edn (CSIRO Publishing: Melbourne)

Juarez S, Nunan N, Duday A-C, Pouteau V, Cheunu C (2013) Soil carbon mineralisation responses to alterations of microbial diversity and soil structure. Biology and Fertility of Soils 49, 939–948.
Soil carbon mineralisation responses to alterations of microbial diversity and soil structure.Crossref | GoogleScholarGoogle Scholar |

Joergensen RG, Brookes PC (1990) Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 m K2SO4 soil extracts. Soil Biology & Biochemistry 22, 1023–1027.
Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 m K2SO4 soil extracts.Crossref | GoogleScholarGoogle Scholar |

Kandeler E (1996) Protease activity. In ‘Methods in soil biology.’ (Eds F Schinner, E Kandeler, R Ohlinger and R Margesin) pp. 165–168. (Springer: Berlin)

Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils 6, 68–72.
Short-term assay of soil urease activity using colorimetric determination of ammonium.Crossref | GoogleScholarGoogle Scholar |

Kaštovská E, Šantrůčková H (2011) Comparison of uptake of different N forms by soil microorganisms and two wet-grassland plants: A pot study. Soil Biology & Biochemistry 43, 1285–1291.
Comparison of uptake of different N forms by soil microorganisms and two wet-grassland plants: A pot study.Crossref | GoogleScholarGoogle Scholar |

Kelliher FM, Barbour MM, Hunt JE (2005) Sucrose application, soil microbial respiration and evolved carbon dioxide isotope enrichment under contrasting land uses. Plant and Soil 268, 233–242.
Sucrose application, soil microbial respiration and evolved carbon dioxide isotope enrichment under contrasting land uses.Crossref | GoogleScholarGoogle Scholar |

Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biology & Biochemistry 34, 139–162.
The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter.Crossref | GoogleScholarGoogle Scholar |

Koranda M, Schnecker J, Kaiser C, Fuchslueger L, Kitzler B, Stange CF, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2011) Microbial processes and community composition in the rhizosphere of European beech—The influence of plant C exudates. Soil Biology & Biochemistry 43, 551–558.
Microbial processes and community composition in the rhizosphere of European beech—The influence of plant C exudates.Crossref | GoogleScholarGoogle Scholar |

Maguire RO, Sims JT (2002) Measuring agronomic and environmental soil phosphorus saturation and predicting phosphorus leaching with Mehlich 3. Soil Science Society of America Journal 66, 2033–2039.
Measuring agronomic and environmental soil phosphorus saturation and predicting phosphorus leaching with Mehlich 3.Crossref | GoogleScholarGoogle Scholar |

Meier EA, Thorburn PJ, Probert ME (2006) Occurrence and simulation of nitrification in two contrasting sugarcane soils from the Australian wet tropics. Australian Journal of Soil Research 44, 1–9.
Occurrence and simulation of nitrification in two contrasting sugarcane soils from the Australian wet tropics.Crossref | GoogleScholarGoogle Scholar |

Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5, 62–71.
A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite.Crossref | GoogleScholarGoogle Scholar | 11178938PubMed |

Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biology and Fertility of Soils 48, 743–762.
Soil enzymology: classical and molecular approaches.Crossref | GoogleScholarGoogle Scholar |

Nottingham AT, Griffiths H, Chamberlain PM, Stott AW, Tanner EVJ (2009) Soil priming by sugar and leaf-litter substrates: A link to microbial groups. Applied Soil Ecology 42, 183–190.
Soil priming by sugar and leaf-litter substrates: A link to microbial groups.Crossref | GoogleScholarGoogle Scholar |

Nottingham AT, Turner BL, Chamberlain PM, Stott AW, Tanner EVJ (2012) Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry 111, 219–237.
Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility.Crossref | GoogleScholarGoogle Scholar |

Otto R, Mulvaney RL, Khan SA, Trivelin PCO (2013) Quantifying soil nitrogen mineralization to improve fertilizer nitrogen management of sugarcane. Biology and Fertility of Soils 49, 893–904.

Page KL, Bell M, Dalal RC (2013) Changes in total soil organic carbon stocks and carbon fractions in sugarcane systems as affected by tillage and trash management in Queensland, Australia. Soil Research 51, 608–614.
Changes in total soil organic carbon stocks and carbon fractions in sugarcane systems as affected by tillage and trash management in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Parham JA, Deng SP (2000) Detection, quantification and characterization of beta-glucosaminidase activity in soil. Soil Biology & Biochemistry 32, 1183–1190.
Detection, quantification and characterization of beta-glucosaminidase activity in soil.Crossref | GoogleScholarGoogle Scholar |

Pedersen H, Dunkin K, Firestone M (1999) The relative importance of autotrophic and heterotrophic nitrification in a conifer forest soil as measured by15N tracer and pool dilution techniques. Biogeochemistry 44, 135–150.
The relative importance of autotrophic and heterotrophic nitrification in a conifer forest soil as measured by15N tracer and pool dilution techniques.Crossref | GoogleScholarGoogle Scholar |

Prober SM, Thiele KR, Lunt ID, Koen TB (2005) Restoring ecological function in temperate grassy woodlands: manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns. Journal of Applied Ecology 42, 1073–1085.
Restoring ecological function in temperate grassy woodlands: manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns.Crossref | GoogleScholarGoogle Scholar |

Richards AE, Brackin R, Lindsay DAJ, Schmidt S (2012) Effect of fire and tree-grass patches on soil nitrogen in Australian tropical savannas. Austral Ecology 37, 668–677.
Effect of fire and tree-grass patches on soil nitrogen in Australian tropical savannas.Crossref | GoogleScholarGoogle Scholar |

Robertson FA, Thorburn PJ (2007) Decomposition of sugarcane harvest residue in different climatic zones. Australian Journal of Soil Research 45, 1–11.
Decomposition of sugarcane harvest residue in different climatic zones.Crossref | GoogleScholarGoogle Scholar |

Robinson N, Brackin R, Vinall K, Soper F, Holst J, Gamage H, Paungfoo-Lonhienne C, Rennenberg H, Lakshmanan P, Schmidt S (2011) Nitrate paradigm does not hold up for sugarcane. PLoS ONE 6, e19045
Nitrate paradigm does not hold up for sugarcane.Crossref | GoogleScholarGoogle Scholar | 21552564PubMed |

Rowell MJ (1995) Colorimetric method for CO2 measurement in soils. Soil Biology & Biochemistry 27, 373–375.
Colorimetric method for CO2 measurement in soils.Crossref | GoogleScholarGoogle Scholar |

Ruwanza S, Musil CF, Esler KJ (2012) Sucrose application is ineffectual as a restoration aid in a transformed southern African lowland fynbos ecosystem. South African Journal of Botany 80, 1–8.
Sucrose application is ineffectual as a restoration aid in a transformed southern African lowland fynbos ecosystem.Crossref | GoogleScholarGoogle Scholar |

Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology & Biochemistry 35, 549–563.
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model.Crossref | GoogleScholarGoogle Scholar |

Sichter NJ, Whiteing C, Bonaventura P (2005) Estimation of harvester losses by determination of sugar in harvest residue. Proceedings of the Australian Society of Sugar Cane Technologists 27, 75–82.

Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Science Society of America Journal 70, 555–569.
Bacterial and fungal contributions to carbon sequestration in agroecosystems.Crossref | GoogleScholarGoogle Scholar |

Swift MJ (1997) Biological management of soil fertility as a component of sustainable agriculture: perspectives and prospects with particular reference to tropical regions. In ‘Soil ecology in sustainable agricultural systems.’ (Eds L Brussaard, R Ferrera-Cerrato) pp. 137–160. (Lewis Publishers: Boca Raton, FL)

Szili-Kovács T, Török K, Tilston EL, Hopkins DW (2007) Promoting microbial immobilization of soil nitrogen during restoration of abandoned agricultural fields by organic additions. Biology and Fertility of Soils 43, 823–828.
Promoting microbial immobilization of soil nitrogen during restoration of abandoned agricultural fields by organic additions.Crossref | GoogleScholarGoogle Scholar |

Vancov T, Keen B (2009) Rapid isolation and high-throughput determination of cellulase and laminarinase activity in soils. Journal of Microbiological Methods 79, 174–177.
Rapid isolation and high-throughput determination of cellulase and laminarinase activity in soils.Crossref | GoogleScholarGoogle Scholar | 19723545PubMed |

Whiteing C (2004) Cutting our losses – how to reduce profits lost in the harvest process. In ‘BSES Bulletin. Vol. 4’. pp. 21–23. (BSES Ltd: Indooroopilly, Qld)

Zhang J, Müller C, Zhu T, Cheng Y, Cai Z (2011) Heterotrophic nitrification is the predominant NO 3 − production mechanism in coniferous but not broad-leaf acid forest soil in subtropical China. Biology and Fertility of Soils 47, 533–542.
Heterotrophic nitrification is the predominant NO 3 − production mechanism in coniferous but not broad-leaf acid forest soil in subtropical China.Crossref | GoogleScholarGoogle Scholar |