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.
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.
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.
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.
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.
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.
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.
Dubach M and Russelle M P 1994 Forage legume roots and nodules and their role in nitrogen transfer. Agron. J. 86, 259-266.
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.
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.
Goins G D and Russelle M P 1996 Fine root demography in alfalfa (Medicago sativa L.). Plant Soil 185, 281-291.
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.
Hendrey G R, Lewin K F and Nagy J 1993 Free air carbon dioxide enrichment: development, progress, results. Vegetatio 104-105, 17-31.
Hodge A 1996 Impact of elevated CO2 on mycorrhizal associations and implications for plant growth. Biol. Fertil. Soils 23, 388-398.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Niklaus P A 1998 Effects of elevated atmospheric CO2 on soil microbiota in calcareous grassland. Global Change Biol. 4, 451-458.
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.
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.
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.
O'Neill E G 1994 Responses of soil biota to elevated atmospheric carbon dioxide. Plant Soil 165, 55-65.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Sadowsky M J and Schortemeyer M 1997 Soil microbial responses to increased concentrations of atmospheric CO2. Global Change Biol. 3, 217-224.
SAS Institute 1987 SAS/STAT guide for personal computers, Version 6 Edition. SAS Institute, Cary, NC pp 549-640. ISBN 1-55544-064-9.
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.
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.
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.
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.
Vestal J R and White D C 1989 Lipid analysis in microbial ecology. BioScience 39, 535-541.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Rights 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
Issue Date:
DOI: https://doi.org/10.1023/A:1019901828483