Skip to main content
Log in

Changes in microbial activity and composition in a pasture ecosystem exposed to elevated atmospheric carbon dioxide

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Elevated atmospheric CO2 increases aboveground plant growth and productivity. However, carbon dioxide-induced alterations in plant growth are also likely to affect belowground processes, including the composition of soil biota. We investigated the influence of increased atmospheric CO2on bacterial numbers and activity, and on soil microbial community composition in a pasture ecosystem under Free-Air Carbon Dioxide Enrichment (FACE). Composition of the soil microbial communities, in rhizosphere and bulk soil, under two atmospheric CO2 levels was evaluated by using phospholipid fatty acid analysis (PLFA), and total and respiring bacteria counts were determined by epifluorescence microscopy. While populations increased with elevated atmospheric CO2 in bulk soil of white clover (Trifolium repens L.), a higher atmospheric CO2 concentration did not affect total or metabolically active bacteria in bulk soil of perennial ryegrass (Lolium perenne L.). There was no effect of atmospheric CO2 on total bacteria populations per gram of rhizosphere soil. The combined effect of elevated CO2 on total root length of each species and the bacterial population in these rhizospheres, however, resulted in an 85% increase in total rhizosphere bacteria and a 170% increase in respiring rhizosphere bacteria for the two plant species, when assessed on a per unit land area basis. Differences in microbial community composition between rhizosphere and bulk soil were evident in samples from white clover, and these communities changed in response to CO2 enrichment. Results of this study indicate that changes in soil microbial activity, numbers, and community composition are likely to occur under elevated atmospheric CO2, but the extent of those changes depend on plant species and the distance that microbes are from the immediate vicinity of the plant root surface.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bazzaz F A 1990 The response of natural ecosystems to the rising global CO2 levels. Annu. Rev. Ecol. Syst. 21, 167-196.

    Google Scholar 

  • Berntson G and Bazzaz F 1997 Nitrogen cycling in microcosms of yellow birch exposed to elevated CO2: simultaneous positive and negative below-ground feedbacks. Global Change Biol. 3, 247-258.

    Google Scholar 

  • Cotrufo M F and Gorissen A 1997 Elevated CO2 enhances belowground C allocation in three perennial grass species at different level of N availability. New Phytol. 137, 421-431.

    Google Scholar 

  • Cotrufo M F, Ineson P and Rowland A P 1994 Decomposition of tree leaf litters grown under elevated CO2: effect of litter quality. Plant Soil 163, 121-130.

    Google Scholar 

  • Dhillion S S, Roy J and Abrams M 1996 Assessing the impact of elevated CO2 on soil microbial activity in aMediterranean model ecosystem. Plant Soil 187, 333-342.

    Google Scholar 

  • Díaz S, Grime J P, Harris J and McPherson E 1993 Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364, 616-617.

    Google Scholar 

  • Dubach M and Russelle M P 1994 Forage legume roots and nodules and their role in nitrogen transfer. Agron. J. 86, 259-266.

    Google Scholar 

  • Federle T W 1986 Microbial distribution in soil new techniques. In Perspectives in Microbial Ecology. Eds F Megusar and M Gantar. pp 493-498. Slovene Society of Microbiology, Ljubljana.

    Google Scholar 

  • Frostegard A, Bååth E and Tunlid A 1993 Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol. Biochem. 25, 723-730.

    Google Scholar 

  • Goins G D and Russelle M P 1996 Fine root demography in alfalfa (Medicago sativa L.). Plant Soil 185, 281-291.

    Google Scholar 

  • Griffiths B S, Ritz K, Ebblewhite N, Paterson E and Killham K 1998 Ryegrass rhizosphere microbial community structure under elevated carbon dioxide concentrations, with observations on wheat rhizosphere. Soil Biol. Biochem. 30, 315-321.

    Google Scholar 

  • Hendrey G R, Lewin K F and Nagy J 1993 Free air carbon dioxide enrichment: development, progress, results. Vegetatio 104-105, 17-31.

    Google Scholar 

  • Hodge A 1996 Impact of elevated CO2 on mycorrhizal associations and implications for plant growth. Biol. Fertil. Soils 23, 388-398.

    Google Scholar 

  • Hodge A, Paterson E, Grayston S J, Campbell C D, Ord B G and Killham K 1998 Characterization and microbial utilization of exudate material from the rhizosphere of Lolium perenne grown under CO2 enrichment. Soil Biol. Biochem. 30, 1033-1043.

    Google Scholar 

  • Hungate B A, Canadell J and Stuart Chapin III F 1996 Plant species mediate changes in soil microbial N in response to elevated CO2. Ecology 77, 2505-2515.

    Google Scholar 

  • Jones T H, Thompson L J, Lawton J H, Bezemer T M, Bardgett R D, Blackburn T M, Bruce K D, Cannon P F, Hall G S, Hartley S E, Howson G, Jones C G, Kampichler C, Kandeler E and Ritchie D A 1998 Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science 280, 441-443.

    Google Scholar 

  • Kimball B A, Mauney J R, Nakayama F S and Idso S B 1993 Effects of increasing CO2 on vegetation. Vegetatio 104/105, 65-75.

    Google Scholar 

  • King A W, Emanuel W R and Post W M 1992 Projecting future concentrations of atmospheric CO2 with global carbon cycle models: the importance of simulating historical changes. Environ. Man. 16, 91-108.

    Google Scholar 

  • Kingsley M T and Bohlool B B 1981 Release of Rhizobium spp. from tropical soils and recovery for immunofluorescence enumeration. Appl. Environ. Microbiol. 42, 241-248.

    Google Scholar 

  • Kropppenstedt R M 1985 Fatty acids and menaquinone analysis of actinomycetes and related organisms. In Chemical Methods in Bacterial Systematics. Eds. M Goodfellow and D E Minnikin. pp 173-199. Academic Press, London.

    Google Scholar 

  • Lamborg M R, Hardy R W F and Paul E A 1983 Microbial effects. In CO2 and plants: The Response of Plants to Rising Levels of Atmospheric Carbon Dioxide. Ed. E R Lemon. pp. 131-176. American Association Adv Science, West-view Press, Boulder, CO. USA.

    Google Scholar 

  • Lewin K F, Hendrey G R, Nagy J and Lamorte R L 1994 Design and application of a free-air carbon dioxide facility. Agric. For. Meteor. 70, 15-29.

    Google Scholar 

  • Luscher A, Hartwig U A, Suter D and Nösberger J 2000 Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Global Change Biol. 6, 655-662.

    Google Scholar 

  • Marilley L, Hartwig U A and Aragno M 1999 Influence of an elevated atmospheric CO2 content on soil and rhizosphere bacterial communities beneath Lolium perenne and Trifolium repens under field conditions. Microb. Ecol. 38, 39-49.

    PubMed  Google Scholar 

  • Merckx R, Dijkstra A, den Hartog A and van Veen J A 1987 Production of root-derived material and associated microbial growth in soil at different nutrient levels. Biol. Fertil.Soils5, 126-132.

    Google Scholar 

  • Montealegre C M, van Kessel C, Blumenthal J M, Hur H, Hartwig U A and Sadowsky M J 2000 Elevated Atmospheric CO2 Alters Microbial Population Structure in a Pasture Ecosystem. Global Change Biol. 6, 475-482.

    Google Scholar 

  • Mousseau M and Saugier B 1992 The direct effect of increased CO2 on gas exchange and growth of forest tree species. J. Exp. Bot.43, 1121-1130.

    Google Scholar 

  • Niklaus P A and Körner C 1996 Responses of soil microbiota of a late successional alpine grassland to long term CO2 enrichment. Plant Soil, 184, 219-229.

    Google Scholar 

  • Niklaus P A 1998 Effects of elevated atmospheric CO2 on soil microbiota in calcareous grassland. Global Change Biol. 4, 451-458.

    Google Scholar 

  • Nitschelm J J, Lüscher A, Hartwig U A and van Kessel C 1997 Using stable isotopes to determine soil carbon input differences under ambient and elevated atmospheric CO2 conditions. Global Change Biol. 3, 411-416.

    Google Scholar 

  • O'Leary W M and Wilkinson S G 1988 Gram-positive bacteria. In Microbial Lipids. Eds. C Ratledge and S G Wilkinson. Vol. 1 pp 117-201. Academic Press, London.

    Google Scholar 

  • O'Neill E G, Luxmoore R J and Norby R J 1987 Elevated atmospheric CO2 effects on seedling growth, nutrient uptake, and rhizosphere bacterial populations. Plant Soil 104, 3-11.

    Google Scholar 

  • O'Neill E G 1994 Responses of soil biota to elevated atmospheric carbon dioxide. Plant Soil 165, 55-65.

    Google Scholar 

  • Paterson E, Hall J M, Rattray E A S, Griffiths B S, Ritz K and Killham K 1997 Effect of elevated CO2 on rhizosphere carbon flow and soil microbial processes. Global Change Biol. 3, 363-377.

    Google Scholar 

  • Paterson E, Rattray E A S and Killham K 1996 Effect of elevated atmospheric CO2 concentration on C-partitioning and rhizosphere C-flow for three plant species. Soil Biol. Biochem. 28, 195-201.

    Google Scholar 

  • Rattray E A S, Paterson E and Killham K 1995 Characterization of the dynamics of C-partitioning within Lolium perenne and to the rhizosphere microbial biomass using 14C pulse chase. Biol. Fert. Soils 19, 280-286.

    Google Scholar 

  • Reasoner D J and Geldreich E E 1985 A new medium for the enumeration and subculture of bacteria from potable water. Appl. Environ. Microbiol. 49, 1-7.

    PubMed  Google Scholar 

  • Rice C W, Garcia F O, Hampton C O and Owensby C E 1994 Soil microbial response in tallgrass prairie to elevated CO2. Plant Soil 165, 67-74.

    Google Scholar 

  • Rillig M C and Allen M F 1998 Arbuscular mycorrhizae of Gutierrezia sarothrae and elevated carbon dioxide: evidence for shifts in C allocation to and within the mycobiont. Soil Biol. Biochem. 30, 2001-2008.

    Google Scholar 

  • Ringelberg D B, Stair J O, Almeida J, Norby R J, O'Neil E G and White D C 1997 Consequences of rising atmospheric carbon dioxide levels for the belowground microbiota associated with white oak. J. Environ. Qual. 26, 495-503.

    Google Scholar 

  • Rodriguez G G, Phipps D, Ishiguro K and Ridgway H F 1992 Use of a fluorescent redox probe for direct visualization of actively respiring bacteria. Appl. Environ. Microbiol. 58, 1801-1808.

    PubMed  Google Scholar 

  • Rogers H H, Prior S A and O'Neill E G 1992 Cotton root and rhizosphere responses to free-air CO2 enrichment. Crit. Rev. Plant Sci. 11, 251-263.

    Google Scholar 

  • Rogers H H, Runion G B and Krupa S V 1994 Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environ. Pollut. 83, 155-189.

    Article  PubMed  Google Scholar 

  • Rotty R M and Marland G 1986 Fossil fuel combustion: recent amounts, patterns, and trends of CO2. In The Changing Carbon Cycle: a Global Analysis. Eds. J R Trabalka and D E Reichle. pp 474-490. Springer-Verlag, New York.

    Google Scholar 

  • Rouhier H and Read D J 1999 Plant and fungal responses to elevated atmospheric CO2in mycorrhizal seedlings of Betula pendula. Environ. Exp. Bot. 42, 231-241.

    Google Scholar 

  • Runion G B, Curl E A, Rogers H H, Backman P A, Rodríguez-Kabana R and Helms B E 1994 Effects of CO2 enrichment on microbial populations in the rhizosphere and phyllosphere of cotton. Agric. For. Meteorol. 70, 117-130.

    Google Scholar 

  • Sadowsky M J and Schortemeyer M 1997 Soil microbial responses to increased concentrations of atmospheric CO2. Global Change Biol. 3, 217-224.

    Google Scholar 

  • SAS Institute 1987 SAS/STAT guide for personal computers, Version 6 Edition. SAS Institute, Cary, NC pp 549-640. ISBN 1-55544-064-9.

    Google Scholar 

  • Schortemeyer M, Dijkstra P, Johnson D W and Drake B G 2000 Effects of elevated atmospheric CO2 concentration on C and N pools and rhizosphere processes in a Florida scrub oak community. Global Change Biol. 6, 383-391.

    Google Scholar 

  • Schortemeyer M, Hartwig U A, Hendrey G R and Sadowsky M J 1996 Microbial community changes in the rhizosphere of white clover and perennial ryegrass exposed to free air carbon dioxide enrichment (FACE). Soil Biol. Biochem. 28, 1717-1724.

    Article  Google Scholar 

  • Tunlid A and White D C 1991 Biochemical analysis of biomass, community structure, nutritional status, and metabolical activity of microbial communities in soil. Soil Biol. Biochem. 7, 229-262.

    Google Scholar 

  • van Veen J A, Liljeroth E and Lekkerkerk L J A 1991 Carbon fluxes in plant-soil systems at elevated atmospheric CO2 levels. Ecol. Appl. 1, 175-181.

    Google Scholar 

  • Vestal J R and White D C 1989 Lipid analysis in microbial ecology. BioScience 39, 535-541.

    Google Scholar 

  • Whipps J M 1985 Effects of CO2 concentration on growth, carbon distribution and loss of carbon from the roots of maize. J. Exp. Bot. 36, 645-651.

    Google Scholar 

  • Zak D R, Pregitzer K S, Curtis, P S and Holmes W E 2000 Atmospheric CO2 and the composition and function of soil microbial communities. Ecol. Appl. 10, 47-59.

    Google Scholar 

  • Zak D R, Pregitzer K S, Curtis P, Teeri J A, Fogel R and Randlett D L 1993 Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles in forested ecosystems. Plant Soil 151, 105-117.

    Google Scholar 

  • Zak D R, Ringelberg D B, Pregitzer K S, Randlett D L, White D C and Curtis, P S 1996 Soil microbial communities beneath Populus Grandidentata grown under elevated atmospheric CO2. Ecol. Appl. 61, 257-262.

    Google Scholar 

  • Zogg G P, Zak D R, Ringelberg D B, Macdonald N W, Pregitzer KS and White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci. Soc. Am. J.61, 475-481.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Montealegre, C.M., van Kessel, C., Russelle, M.P. et al. Changes in microbial activity and composition in a pasture ecosystem exposed to elevated atmospheric carbon dioxide. Plant and Soil 243, 197–207 (2002). https://doi.org/10.1023/A:1019901828483

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1019901828483

Navigation