Skip to main content
SpringerLink
Log in

Unraveling the role of hyphal networks from arbuscular mycorrhizal fungi in aggregate stabilization of semiarid soils with different textures and carbonate contents

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Our study was intended to elucidate the involvement of three species of arbuscular mycorrhizal fungi (AMF) in the formation and stabilization of aggregates in semiarid soils with different textures and calcium carbonate contents.

Methods

We used a root-hyphae compartment approach to compare the effect of three AMF (Rhizophagus irregularis, Septoglomus deserticola, and Gigaspora gigantea) on the structural stability of the hyphosphere (root-free hyphae) and mycorrhizosphere (hyphae + root) soil of Olea europaea plants grown in two soils differing in their texture (sandy loam and silty loam) and calcium carbonate content.

Results

Only the R. irregularis strain significantly increased the percentage of stable aggregates in both types of soil, being the increases higher in the hyphosphere compartment (on average, about 30 % compared to non-inoculated soil). In the hyphosphere compartment of both soils, the hyphal length developed by plants inoculated with R. irregularis was 81 % greater than that of non-inoculated plants. The effect of the AMF on soil aggregation was mediated by mechanical entanglement of mycorrhizal fungal hyphae but without a contribution of labile carbohydrates.

Conclusion

The ability of extraradical hyphae to improve soil structure was independent of the soil texture and content of carbonates.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Asano M, Wagai R (2014) Evidence of aggregate hierarchy at micro- to submicron scales in an allophanic Andisol. Geoderma 216:62–74

    Article  CAS  Google Scholar 

  • Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41:1491–1496

    Article  CAS  Google Scholar 

  • Black CA, Evans DD, White JL, Ensminger LE, Clark FE (1965) Methods of soil analysis. Part 2. ASA and SSSA, Madison, Wisconsin, USA

  • Brink RH, Dubach P, Lynch DL (1960) Measurements of carbohydrates in soil hydrolyzates with anthrone. Soil Sci 89:157–166

    Article  CAS  Google Scholar 

  • Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22

    Article  CAS  Google Scholar 

  • Caravaca F, Barea JM, Figueroa D, Roldán A (2002a) Assessing the effectiveness of mycorrhizal inoculation and soil compost addition for enhancing reafforestation with Olea europaea subsp. sylvestris through changes in soil biological and physical parameters. Appl Soil Ecol 20:107–118

    Article  Google Scholar 

  • Caravaca F, Hernández T, García C, Roldán A (2002b) Improvement of rhizosphere aggregate stability of afforested semiarid plant species subjected to mycorrhizal inoculation and compost addition. Geoderma 108:133–144

    Article  CAS  Google Scholar 

  • Caravaca F, Lax A, Albaladejo J (2004) Aggregate stability and carbon characteristics of particle-size fractions in cultivated and forested soils of semiarid Spain. Soil Till Res 78:83–90

    Article  Google Scholar 

  • Caravaca F, Alguacil MM, Barea JM, Roldán A (2005) Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem. Soil Biol Biochem 37:227–233

    Article  CAS  Google Scholar 

  • Chenu C, Le Bissonnais Y, Arrouays D (2000) Organic matter influence on clay wettability and soil aggregate stability. Soil Sci Soc Am J 64:1479–1486

    Article  CAS  Google Scholar 

  • Chivenge P, Vanlauwe B, Gentile R, Six J (2011) Comparison of organic versus mineral resource effects on short-term aggregate carbon and nitrogen dynamics in a sandy soil versus a fine textured soil. Agric Ecosyst Environ 140:361–371

    Article  CAS  Google Scholar 

  • Daynes CN, Field DJ, Saleeba JA, Cole MA, McGee PA (2013) Development and stabilisation of soil structure via interactions between organic matter, arbuscular mycorrhizal fungi and plant roots. Soil Biol Biochem 57:683–694

    Article  CAS  Google Scholar 

  • Degens BP, Sparling GP, Abbott LK (1996) Increasing the length of hyphae in a sandy soil increases the amount of water-stable aggregates. Appl Soil Ecol 3:149–159

    Article  Google Scholar 

  • Fernández C, Alonso C, Babín MM, Pro J, Carbonell G, Tarazona JV (2004) Ecotoxicological assessment of doxycycline in aged pig manure using multispecies soil systems. Sci Total Environ 323:63–69

    Article  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–499

    Article  Google Scholar 

  • Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13

    Article  CAS  PubMed  Google Scholar 

  • Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 374:523–537

    Article  CAS  Google Scholar 

  • Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: molecular biology and physiology. Kluwer, Dordrecht, pp 3–18

    Chapter  Google Scholar 

  • Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphae production of vesicular-arbuscular mycorrhizal fungi in pasture and tail grass prairie communities. Oecologia 103:17–23

    Article  Google Scholar 

  • Muthukumar T, Udaiyan K (2000) Influence of organic manures on arbuscular mycorrhizal fungi associated with Vigna unguiculata (L.) Walp. in relation to tissue nutrients and soluble carbohydrate in roots under field conditions. Biol Fertil Soils 31:114–120

    Article  Google Scholar 

  • Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337

    Article  CAS  Google Scholar 

  • Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377–400

    Article  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Piotrowski JS, Denich T, Klironomos JN, Graham JM, Rillig MC (2004) The effects of arbuscular mycorrhizas on soil aggregation depend on the interaction between plant and fungal species. New Phytol 164:365–373

    Article  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 17:41–53

    Article  Google Scholar 

  • Rillig MC, Field CB, Allen MF (1999) Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands. Oecologia 119:572–577

    Article  Google Scholar 

  • Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42:1189–1191

    Article  CAS  Google Scholar 

  • Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388

    Article  CAS  PubMed  Google Scholar 

  • Roldán A, García-Orenes F, Lax A (1994) An incubation experiment to determine factors involving aggregation changes in an arid soil receiving urban refuse. Soil Biol Biochem 26:1699–1707

    Article  Google Scholar 

  • Roldán A, Carrasco L, Caravaca F (2006) Stability of desiccated rhizosphere soil aggregates of mycorrhizal Juniperus oxycedrus grown in a desertified soil amended with a composted organic residue. Soil Biol Biochem 38:2722–2730

    Article  Google Scholar 

  • Schreiner RP, Mihara KL, McDaniel H, Bethlenfalvay GJ (1997) Mycorrhizal fungi influence plant and soil functions and interactions. Plant Soil 188:199–209

    Article  CAS  Google Scholar 

  • Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176

    Article  CAS  Google Scholar 

  • Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota and soil organic matter dynamics. Soil Till Res 79:7–31

    Article  Google Scholar 

  • Skidmore EL, Layton JB (1992) Dry-soil aggregate stability as influenced by selected soil properties. Soil Sci Soc Am J 56:557–561

    Article  Google Scholar 

  • SSS (2010) Keys to Soil Taxonomy, first Ed. USDA. Natural Resources Conservation Service, Washington DC

  • Tisdall JM (1994) Possible role of soil-microorganisms in aggregation in soils. Plant Soil 159:115–121

    Article  Google Scholar 

  • Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. J Soil Sci 33:141–163

    Article  CAS  Google Scholar 

  • Torrecillas E, Alguacil MM, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78:6180–6186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Virto I, Gartzia-Bengoetxea N, Fernandez-Ugalde O (2011) Role of organic matter and carbonates in soil aggregation estimated using laser diffractometry. Pedosphere 21:566–572

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Seneca Foundation (Project FS-11828/PI/09). The authors wish to thank Dr. D.J. Walker for the English revision.

Author information

Authors and Affiliations

  1. Institut für Biologie, Plant Ecology, Freie Universität Berlin, Altensteinstr. 6, 14195, Berlin, Germany

    J. Kohler

  2. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), 14195, Berlin, Germany

    J. Kohler

  3. Department of Soil and Water Conservation, CSIC-Centro de Edafología y Biología Aplicada del Segura, P.O. Box 164, Campus de Espinardo, 30100, Murcia, Spain

    A. Roldán, M. Campoy & F. Caravaca

Authors
  1. J. Kohler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Roldán
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Campoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Caravaca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Caravaca.

Additional information

Responsible Editor: Tatsuhiro Ezawa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kohler, J., Roldán, A., Campoy, M. et al. Unraveling the role of hyphal networks from arbuscular mycorrhizal fungi in aggregate stabilization of semiarid soils with different textures and carbonate contents. Plant Soil 410, 273–281 (2017). https://doi.org/10.1007/s11104-016-3001-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3001-3

Keywords

Search

Navigation