R.C.Suelo Nutr. Veg. 8 (2) 2008 (9-18) J. Sc. Plant Nutr. 8 (2) 2008 (9-18) 9

ARBUSCULAR MYCORRHIZAL FUNGI AND SOIL AGGREGATION

Fernando Borie, Rosa Rubio, Alfredo Morales Universidad de La Frontera. Casilla 54-D-Temuco. Corresponding author: [email protected]

Hongos micorrícicos arbusculares y agregación de suelo

Keywords: arbuscular mycorrhizal fungi, soil aggregates, glomalin.

ABSTRACT

Soil aggregation is governed by several biotic and abiotic components including land- use management. Aggregation is essential to maintain soil physical properties and facilitate biogeochemical cycling. Hyphae of arbuscular mycorrhizal fungi (AMF) are considered to be primary soil aggregators and there is a positively correlation between AMF hyphae and aggregate stability in natural systems. Recent evidence suggests that glomalin (GRSP), a glycoprotein produced by AMF hyphae which has a cementing capacity to maintain soil particles together, is mainly involved in such aggregation. However, recently controversial results together with reported shortcoming in glomalin determinat suggest to proceed with caution when studying glomalin in connection with soil aggregation. Relationships between glomalin and soil aggregates found in Chilean are discussed. 10 Arbuscular mycorrhizal fungi, Borie et al.

Palabras Claves: Hongos micorrícicos, agregados de suelo, glomalina.

RESUMEN

La agregación de suelo es gobernada por una serie de factores bióticos y abióticos incluyendo el manejo del suelo. La agregación es fundamental para mantener las propiedades físicas del suelo y facilitar los ciclos biogeoquímicos. Las hifas de los hongos formadores de micorrizas arbusculares (MA) son consideradas como importantes agentes aglutinadores de partículas del suelo y se han descrito correlaciones positivas entre hifas de hongos MA y estabilidad de agregados en sistemas naturales. Recientemente existen evidencias que sugieren que la glomalina (GRSP), una glicoproteína producida en gran cantidad por las hifas de los hongos MA y que tiene una capacidad cementante de las partículas de suelo, está fuertemente involucrada en dicha agregación. Sin embargo, resultados contradictorios obtenidos recientemente junto con problemas reportadas en la determinación de glomalina sugieren proceder con cautela cuando se relaciona la glomalina con respecto a la agregación del suelo. Se discuten interrelaciones encontradas en suelos chilenos entre glomalina y agregados del suelo.

INTRODUCTION

Soil structure exerts important influences with the consolidation of soil particles into on the functioning of soil, its ability to microaggregates (< 250 µm) and further support plant and animal life, controlling formation of macroaggregates (>250 µm). environmental quality with especial The mechanism involved in soil emphasis on soil C sequestration, nutrient aggregation is complex but in general is and gas fluxes and water quality. Soil viewed as microaggregates being formed structure is often expressed as the degree from organic molecules tied to clay and of stability of aggregates being a major polycations, which in turn are linked with factor which moderates physical, chemical, other microaggregates to form and biological processes leading the soil macroaggregates. Briefly, aggregation is dynamics (Bronick and Lal, 2005). Soil the result of rearrangement, flocculation aggregates results from a combination of and cementation of soil particles where soil primary mineral particles with organic and organic carbon, polycations, clay, minerals inorganic materials. This process, dynamic and, especially biota are playing a key role. and complex, is influenced in turn by the Here, we will describe shortly the principal interaction of several factors including factors involved in soil aggregates formation environmental components, soil with specially attention to the soil management, plant effects but largely by components involved in plant growth and soil properties. Among these the most microbial development. Readers who want significant are moisture availability, mineral to deep in this topic may read some composition, soil texture, the quantity and interesting recent reviews (Bronick and Lal, quality of SOM, microbial and enzyme 2005; Rillig and Mummey, 2006) and other activities, mineral nutrients and others such specific papers related to (Six as polycations, etc. Soil aggregation, begins et al., 1999; 2000). R.C.Suelo Nutr. Veg. 8 (2) 2008 (9-18) J. Soil Sc. Plant Nutr. 8 (2) 2008 (9-18) 11

Soil properties contributing to soils carbon is mainly constituted by humic aggregation substances (Aguilera et al., 1997). On the other hand, particulate organic Soil organic carbon fraction matter (POM) constituted by large particles Soil organic carbon produces some of organic matter (250-2000µm) as a light heterogeneous habitats where aggregation fraction, can be considered as free or is more intense. The wide variety on overlayed organic matter on soil particles chemical nature of soil organic compounds which in turn they offer a higher physical determines its formation and decomposition protection against decomposition of POM. rates which induce transient or prolonged Particulate organic matter may be an effects. However, all factors for soil important factor in the formation of aggregates formation are directly or macroaggregates throughout direct binding indirectly related in this process (Chenu action over microaggregates or indirectly et al., 2000). Therefore, the effectthrough on the polysaccharides produced by aggregation of labile sources of organic C microorganisms when metabolizing POM is transient whereas C sources with higher (Jastrow, 1996). stability increase the permanence of such Other important sources of organic effect (Schulten and Leinweber, 2000). compounds on aggregation are Humic substances are believed to be polysaccharides, carbohydrates, lignin and recalcitrant as a result of their chemical lipids. Therefore, the role played by resistance and their interactions with clays carbohydrates is variable depending on its and inorganic soil components conferring source and nature being more resistant to physical protection against microbial decomposition those produced by degradation. For instance, Chorover et al. microorganisms (Bronick and Lal, 2005). (2004) studying a weathering Polysaccharides have a transient effect chronosequence of volcanic soils in Hawaii functioning as bridges to bind soil particles found that aliphatic and aromatic or sometimes acting as glue for maintaining components of organic matter dominate particles together. Chemical nature of lignin humic acids in later stages of soil together with its high recalcitrance, even development (from 150-400 ky). This when its biological stability have been observation is in contrast to wet chemical questioned to be no more than 100 yr analysis showing that lignin, the most (Dignac et al., 2005) suggest a very low important aromatic compounds of soils may direct effect on aggregation; however, in remain in soil only for 100 years (Dignac our experience, where it is common to find et al., 2005). Thus, it may be concluded lignin decomposers, the fungal mycelia favor that the wet chemical techniques to typify the aggregation through hyphal network. extracted from volcanic Lipids, as a cell wall constituent is found in soils is not significant because chemical small amounts in soils (Borie and Barea, fractionation of SOM using alkaline removal 1985), having possibly a very transient effect. does not yield a biological functional fraction Finally, in recent years it has been of soils (Oades, 1988). In spite of this, the described the isolation from soil of a classical concept of aggregation is still being glycoprotein produced by arbuscular used. The coating of particles with such mycorrhizal fungi with a strong cementing recalcitrant materials including humic and capacity of soil particles (Wright and fulvic acids and humins contribute to Upadhyaya, 1996; 1998; Rillig et al., maintain particles together avoiding 2002; Rillig 2004). However, due to degradation processes. These types of the high importance this compound organic compounds are very important in presents it will be described in further organic soils where the bulk of organic paragraphs. 12 Arbuscular mycorrhizal fungi, Borie et al.

Polycations network, although and bacteria have Polyvalent cations such as Al and Fe a significant role as well (Degens, 1997; habitually found in acidic soils improve Tisdall et al., 1997). The role of fungi in soil aggregation through bridges formation soil aggregation can be indirect (or passive) between inorganic minerals or clay and soil due to a physical network of hyphae organic carbon. Aggregates containing clays maintaining soil particles together or directly and Al and Fe oxides or hydroxides promote (active) by cementing capacity of the soil organic C incorporation conferring extracellular compounds released. Among aggregate stability, especially in volcanic this, arbuscular mycorrhizal fungi (AMF) soils. Recently, Matus et al. (2006) have appear to play a predominant effect on demonstrated that soil organic matter aggregates formation because the symbiosis accumulation in Chilean volcanic soils is significantly changes the functioning. produced by Al stabilization rather than They also have a vast and more extensive climatic conditions and clay content of soils. hyphal mycelia in comparison with saprobic Bivalent cations such as Ca and Mg also fungi. In addition, it is known that plant improve soil aggregation in the same way species may differ in their effects on soil as trivalent cations above mentioned. aggregation, in agricultural soils as well as However, in some soils Mg may have a in natural (Eviner and Chapin, deleterious effect on aggregation due to a 2002; Pietrowski et al., 2004) and, higher swelling effect on clays present in consequently, changes in plant community such soils (Zhang and Norton, 2002). are also affecting soil structure. However, Consequently, the use of soil amendments as AMF diversity affects plant community such as lime, gypsum or dolomite can have composition soil aggregated in turn will be significant effects on soil aggregates influenced (van der Heijden et al., 1998). formation. In summary, any event affecting both root development and AMF behavior will affect Clay minerals soil aggregation. Clay minerals influence properties affecting AMF appear to be the most important soil aggregation. As clay interacts with soil fungal mediator of soil aggregation due to: organic carbon and both are intimately a) they represent a dominant soil component related with aggregates, all soil properties accounting for 30% of whole of soil affecting one also affect to the other and microbial biomass (Rillig et al., 1999; soil aggregation as a whole. Thus, pH, CEC, Olsson, 1999); b) carbon supply resources ions and the nature of mineralogy influence for living are coming from the root soil aggregation. In general, aggregation is photosynthates in comparison with saprobic high in high-activity clays (for instance, fungi which depend on limiting carbon doubled layered crystal structure), and soil substrates available in the bulk soil and organic carbon is associated to high CEC. c) there is some evidence that grazers prefer Non-crystalline clay minerals such as saprobic than mycorrhizal hyphae allophane and imogolite, both typic from (Klironomos and Kendrick, 1996) perhaps Chilean volcanic derived soils, with high as a thing of taste resulting in a longer variable charge tend to produce high resilience in the soil. As a consequence, aggregation. Clay type also affect AMF appear as one of the most important decomposition rate of soil organic carbon. components in describing biotic influences on soil aggregation. However, AMF exert Biota a strong influence at the scale of There is consensus that among soil biota, macroaggregates (> 250 µm) in comparison fungi are the most important agents involved with bacteria and archaea which would be in soil aggregation through fungal mycelia expected to influence the formation and R.C.Suelo Nutr. Veg. 8 (2) 2008 (9-18) J. Soil Sc. Plant Nutr. 8 (2) 2008 (9-18) 13 stabilization of microaggregates in a more (Wright and Upadhyaya, 1996). The direct way (Rillig and Mummey, 2006). extraction of glomalin from plant hyphae Recently, a new factor and perhaps with and soils is extremely drastic. In fact, it is greater incidence in soil aggregation was the severity of the extraction conditions that discovered and described by Wright and clearly demonstrates its uncommonly high Upadhyaya (1996) named glomalin which stability. Glomalin is very difficult to is copiously produced by AMF. solubilize and it is resistant to most chemical used in routine and characterization methods Glomalin (Wright and Upadhyaya, 1996). For this In recent years it has been described a reason is though that glomalin is lost in glycoprotein produced by arbuscular humin fraction when applying the mycorrhizal fungi with a strong cementing traditional method for soil humic compounds capacity of soil particles (Wright and fractionation (Nichols Wright, 2005) but Upadhyaya, 1996; 1998; Rillig et al., 2002; our research group have not found significant Rillig 2004). Prior to 1996, the influences amounts of glomalin in humin fractions of AMF in aggregation were not clearly from Chilean andisols and ultisols (Borie understood and the sources of carbon et al., unpublished). The basic extraction compounds involved in aggregate method of glomalin involves the use of a stabilization were not known in spite of citrate buffer at neutral or slight alkaline early reports of Gupta and Germida (1988), pH at high temperature. It has been Miller and Jastrow (1990) and Haynes and postulated two glomalin fractions which Swift (1990) who suggested the possibility differ in extraction conditions from soils. that AMF was involved in soil aggregation The easily extractable glomalin (EEG) is but not showing clear evidences on that. determinated autoclaving 1 g of soil mixed It is now known that glomalin is present with 20 mM citrate at pH 7.0 for 30-60 in large amounts in soils which is indeed a min. The solution containing solubilized distinct component of soil organic matter. glomalin is separated by centrifugation at This is a glycoprotein from Glomales which 10000 x g for 10 min. Total glomalin (TG) is the taxonomic genera to which AMF is determined by an exhaustive extracction belong (Wright and Upadhyaya, 1996). with 50 mM citrate solution at pH 8.0 for Axenic cultures show that glomalin, 60 min in autoclave. In each fraction the originally present in AMF wall hyphae in a protein is quantified in a spectrophotometer 80% according Driver et al., ( 2005) and using the Bradford assay. Table 1 shows secreted into the environment in a minor the correlation coefficients for EEG and TG proportion (Rillig and Mummey, 2006), is on several properties among then soil accumulated in air-water interface (Haddad aggregation in 37 different soils according and Sarkar, 2003). Several studies have Wright and Upadhyaya (1998). Until now, shown that glomalin, aggregate stability and all papers related to glomalin, including soil management are linked (Wright et al., those from different soil types from Chile, 2007). However, some recent studies do not show high relationships between TG and show such close relationships (Pietrowski % soil C and TG and EEG (Borie et al., et al., 2004). 2000). However, we have not found close Glomalin is currently quantified from soil relationships between water stable soil following an operational definition as aggregates (%) and glomalin content in an glomalin-related soil protein (GRSP; Rillig Andisoil (r= 0.26) and a Mollisol (r= 0.11) 2004). The main detection tool is a in comparison with an Alfisol (r= 0.51) or monoclonal antibody (MAb32B11), raised an Ultisol (r= 0.96) (Fig. 1). originally against crushed AMF spores 14 Arbuscular mycorrhizal fungi, Borie et al.

Table 1. Correlation coefficients for fractions of glomalin, % C in soil aggregates, and aggregate stability (Wright and Upadhyaya, 1998).

Cuadro 1. Coeficientes de correlación para fracciones de glomalina, % C en agregados del suelo y estabilidad de agregados (Wright and Upadhyaya, 1998).

** and *** denote significance at p < 0.1 and p < 0.01, respectively.

Figure 1: Relationship between glomalin content-GRSP and water-stable aggregates in different soils from Chile.

Figura 1: Relación entre contenido de glomalina-GRSP y agregados estables al agua en diferentes suelos de Chile. R.C.Suelo Nutr. Veg. 8 (2) 2008 (9-18) J. Soil Sc. Plant Nutr. 8 (2) 2008 (9-18) 15

Soil management and aggregation does. On the opposite, soluble P sources decrease mycorrhizal colonization specially Soil structure can be significantly modified in fertile P soils. through management practices. In this On the other hand, the aggregate dynamics regard, management practices including vary among different crops, crop rotations tillage methods, residue management, and cover crops (Bronick and Lal, 2005). amendment application, soil fertility and The influence of different crops is according crop rotation, among others, can have and to their chemical composition and root enormous influence on soil aggregation and tending to be short-lived under conventional its stability. tillage regimes, (Chan and Heenan, 1996). Tillage disrupts soil aggregates, compact Cover crops increase C inputs, CEC, soil the subsoil and disturb plant and animal aggregate stability and may enhance communities leaving a decrease in soil microbial biomass. The influence of crops organic matter, CEC, microbial and faunal and crop rotation is important on soil activities. Furthermore, root and fungal aggregation due to plant roots and their networks are disrupted decreasing the rhizospheric effects. Roots enmesh, realign stability of soil aggregates and favoring soil particles and release exudates, which leaching, losses of nutrients and erosion. result in physical, chemical and biological Moreover, tillage affects negatively AM alterations that influence soil aggregation fungal mycelia length (Castillo et al., 2006) (Bronick and Lal, 2005). Aggregation tends and also the production of glomalin (Borie to increase with increasing root length et al., 2006) both promoting agents of soil density, microbial association and glomalin, aggregation. The intensity and timing of among other effects (Rillig et al., 2002). tillage will determine the extent to which Aggregate stability is greater in rizosphere the negative effect on soil aggregation can soil tha non-rizosphere soil (Caravac et al., be occurs. 2002) due to an increased rhizodeposition, The addition of compost to soil improves root density, root turnover, hyphal growth, soil structure and lowers the bulk density. microbial biomass, all of them which directly Composting materials can increase or indirectly are influencing in maintaining macroaggregation and rhizospheric particles together. In a recent paper, aggregate stability. The effects of compost Pietrowski et al. (2004) have tested the additions on soil structure may be short- effects of specific plant- combinations lived although these effects are generally on aggregate stability studying whether positive on structural properties (Debosz hyphal length and root biomass determine et al. 2002). It is expected to find a better its stabilization, predicting whether fungi soil structure in soils under organic producing more hyphae, and or plants with agriculture than in soils with conventional higher root biomasses would better stabilize agricultural managements. soils structure. They used nine plant species The complexities of fertilizers and other and five fungus species. The results showed amendments on chemical, physical and that AMF with greater extraradical mycelium biological soil properties results on variable production were represented by the effects on soil aggregation. In general, Gigasporaceae and plants of high root fertilizer application increases soil biomass by grasses. Unfortunately, in this aggregation through an improvement of study, the main related hypothesis to find microbial and faunal activities. Nitrogen an “specialist” AMF fungus which promote and P fertilizers added to unfertile soils such water stable aggregates independent of plant as those poor in available P increase host, was not tested. Until now, the better mycorrhizal activity as well as insoluble is to use a cocktail of AMF in eroded soil sources of phosphate (like rock phosphate) or for application in soil restoration. 16 Arbuscular mycorrhizal fungi, Borie et al.

CONCLUSIONS BORIE, F., RUBIO, R., MORALES, A., CASTILLO, C. 2000. Relación entre Soil structure stability is strongly influenced densidad de hifas de hongos by the nature and content of soil organic micorrizógenos arbusculares y matter. Land use and management practices producción de glomalina con las influencing SOM will be determinant in soil características físicas y químicas de aggregation. Root and fungal hyphae are suelos bajo cero labranza. Rev. Chil. among the most important biotic factors, if Hist.Nat. 73: 749-756. not the most important agents in soil BORIE, F., RUBIO, R., ROUANET,J.L, aggregate stabilization. Given that the MORALES, A., BORIE, G., importance of soil aggregation to the ROJAS,C. 2006. Effects of tillage functioning in the ecosystems and the role systems on soil charactectics, glomalin played by AMF in this context, it is and mycorrhizal propagules in a surprising the lack of studies in connection Chilean Ultisol. Soil Till. Res. 88: 253- with this topic. Last years we have done 261. some efforts for studying the relationships BRONICK, C.J., LAL, R. 2005. Soil between SOM and microbial activity structure and management : a review. including AMF in aggregation of soils in Geoderma 124: 3-22. southern Chile. However, we are aware that CARAVACA, F., HERNÁNDEZ, T., more studies are needed for obtaining a GARCÍA, C., ROLDÁN, A. 2002. better understanding of processes governing Improvement of rhizosphere aggregate the stability of soil aggregates in our volcanic stability of afforested semiarid plant soils. We expect that in vitro glomalin species subjected to mycorrhizal production will be an important tool to face inoculation and compost addition. this challenge. Geoderma 108: 133-144. CASTILLO, C. G., RUBIO, R., ROUANET, AKNOWLEDGEMENTS J.L, BORIE, F. 2006. Early effects of tillage and crop rotation on arbuscular Financial support of Fondecyt 1060372 is mycorrhizal fungal propagules in an acknowledged. We thank Dr. Francisco Ultisol. Biol. Fert. Soils 43: 83-92. Matus from Universidad de La Frontera for CHAN, K.Y., HEENAN, D.P. 1996. The its critical comments on early version of the influence of crop rotation on soil manuscript. structure and soil physical properties under conventional tillage. Soil Till. Res. 37: 113-125. REFERENCES CHENU, C., LE BISSONNAIS, Y., ARROUAYS, D. 2000. Organic matter AGUILERA, S.M., BORIE, G., GALINDO, influence on clay wettability and soil G., PEIRANO, P. 1997. Organic matter aggregate stability. Soil Sci. Soc. Am.J. in volcanic soils in Chile. Chemical 64: 1479-1486. and Biochemical characterization. CHOROVER, J., AMISTADI, M.K., Commun. Soil Sci. Plant Anal. 28: CHADWICK, O.A. 2004. Surface 899-912. charge evolution of mineral-organic BORIE, F., BAREA, J.M. 1985. Occurrence complexes during in of lipid-P in volcanic ash derived soils Hawaiian basalt. Geochim. of Chile. Agrochimica 28: 317-324. Cosmochim. Ac. 68: 4859-4876. R.C.Suelo Nutr. Veg. 8 (2) 2008 (9-18) J. Soil Sc. Plant Nutr. 8 (2) 2008 (9-18) 17

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