MINIREVIEW

Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence Sonia Purin1 & Matthias C. Rillig2,3 1

¨ Berlin, Berlin, Germany; and Division of Plant and Soil Sciences, West Virginia University, Morgantown, WV, USA; 2Institut fur ¨ Biologie, Freie Universitat Division of Biological Sciences, The University of Montana, Missoula, MT, USA

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Correspondence: Sonia Purin, Division of Plant and Soil Sciences, West Virginia University, 1090 Agricultural Sciences Building PO Box 6108, Morgantown, WV 26506-6108, USA. Tel./fax: 11 304 293 8836; e-mail: [email protected] Received 27 September 2007; accepted 25 October 2007. First published online 7 December 2007. DOI:10.1111/j.1574-6968.2007.01007.x Editor: Richard Staples Keywords arbuscular mycorrhizal fungi; microbial parasitism; mycoparasitism; rhizosphere interactions.

Abstract In order to understand the functioning of mycorrhizal fungi in ecosystems it is necessary to consider the full suite of possible biotic interactions in the soil. While a number of such interactions have recently been shown to be crucially important, parasitism is a highly neglected feature in the ecology of arbuscular mycorrhizal fungi (AMF). A number of studies have classified some interactions between populations of bacteria and fungi with AMF as parasitism, generating discussion about its consequences at both ‘parasite’ and host population levels. This paper reviews these various publications , and based on a set of criteria that are necessary to demonstrate parasitism, it was concluded that parasitism has not been conclusively shown to exist in AMF, even though some data are highly suggestive of such a relationship. The difficulties in gathering data supportive of parasitism were discussed, and hypotheses for defense were offered. This paper concludes by presenting potential consequences of AMF parasitism at the population/community levels and by discussing applied aspects.

Introduction Arbuscular mycorrhizal fungi (AMF) establish symbioses with the majority of plant species and influence a number of key processes in terrestrial ecosystems, such as primary productivity, nutrient cycling, and physico-chemical properties of soil (Allen, 1991; Rillig, 2004). In their life cycle, these fungi establish intraradical colonization, and also extend their mycelium biomass into the soil environment, producing over 100 m hyphae g 1 of soil in some ecosystems (Miller et al., 1995; Olsson et al., 1999). The functioning of this extraradical hyphal network is of key importance in mycorrhizal ecology because it represents not only an uptake point for soil nutrients but also a dispersal mechanism and a complex linkage network among roots within a plant community (Miller & Jastrow, 1990; Rillig & Mummey, 2006; Selosse & Duplessis, 2006). It is becoming increasingly clear that interactions of other soil biota with this mycelium should be an integral part of any conceptual model of mycorrhizal functioning. Two examples of biotic interactions that have been explored in considerable detail with AMF (in addition to plant hosts) are hypha-associated bacteria (e.g. Hodge, 2000; Johansson et al., 2004; Rillig

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et al., 2006), including mycorrhiza-helper bacteria (Garbaye, 1994), and consumption of mycelium by grazers (Klironomos & Kendrick, 1996; Klironomos & Ursic, 1997; Klironomos et al., 1999; Johnson et al., 2005; Jonas et al., 2007). The latter example illustrates powerfully how including a biotic interaction could shift the concept of functioning of the symbiosis (Gange, 2000). Therefore it is important to consider the full spectrum of interactions with AMF, which includes possible parasitism of the mycelium. Parasitism is a highly important interaction in many environments, including soils, and some groups of fungi are known to be affected by parasites, i.e. Oomycetes (Inbar et al., 1996; Siwek et al., 1997; Ali-Shtayeh & Saleh, 1999), Ascomycetes (Benyagoub et al., 1998) and Basidiomycetes (Gao et al., 2005), but this interaction still remains to be intensively studied for the Glomeromycota phylum. There are several reasons to expect that these fungi are parasitized. AMF mycelium represents a considerable biomass component in soils (Miller et al., 1995; Olsson et al., 1999), including nutrients en route to the plant, and fatty acid-rich structures (Olsson, 1999; Olsson & Johnson, 2005) – a substantial substrate pool for microorganisms. On the one hand, hyphae are known to have a high turnover rate in

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Parasitism of AMF: reviewing the evidence

soil, of 5–6 days (Staddon et al., 2003); this would perhaps decrease the importance of any parasitism. On the other hand, some parts of an AMF mycelium seem to persist (Olsson & Johnson, 2005); also spores are resting structures packed with lipids (Olsson, 1999), and these structures could serve as points of attack to parasites. Given the strong influence of AMF on terrestrial ecosystems and plant communities, potentially even relatively small effects of parasitism, especially on extraradical hyphae, could translate into important functional consequences. The present synthesis has the goal to draw attention to AMF as a target of parasites. After defining parasitism for AMF, the evidence for potential parasites in different soil biota groups and how they fulfill the criteria of a parasitism relationship were reviewed. This study also presents mechanisms that may regulate these interactions and protect AMF from being parasitized, and concludes by discussing potential consequences of parasitism at both population and ecosystem levels .

General considerations about parasitism applied to AMF According to classical definitions, the term parasitism describes a relationship in which one organism obtains nutrients from another, living in or on its host and reducing its fitness (Jeffries, 1995). However, the application of this concept to filamentous fungi, including AMF, is problematic from an operational perspective owing to the uncertainty of what parameters should be measured in order to assess fitness (reviewed by Pringle & Taylor, 2002). For AMF, parameters that are useful are the number of spores when questioning the persistence and dispersal of a species in a given environment; but either establishment of root colonization or extraradical hyphal growth are more useful when symbiotic efficiency with the host plant is the focal point of fitness. Either way, one or several justifiable fitness parameters should be included in the measurement protocol, and extraradical hyphal length, inoculum potential (i.e. an integrative measure of the ability to colonize roots), and spore production were suggested. It is crucial to separate parasitism from other relationships that may also result in negative effects on AMF, such as competition (when fitness of both species are negatively affected), or where a close association is involved, such as commensalism (when one species benefits, but the other is not affected). An additional challenge is to identify the AMF life history stage that is most likely to be parasitized, namely intraradical mycelium, extraradical hyphae, or spores. This paper assumes that the extraradical mycelium would be more exposed to organism interactions, as the rhizosphere soil environment harbors high densities and diverse microbial populations. However, root tissues could contain miFEMS Microbiol Lett 279 (2008) 8–14

croorganisms that are specialized in parasitizing AMF mycelium. Also, the concentration of elements in intraradical hyphae is usually higher than in root tissues (Rufyikiri et al., 2003), which could turn the mycelium into a target for parasitic attack inside the plant. Also, there is cytoplasmic continuity between extra- and intraradical mycelium (including transport processes), which could present a pathway for invasion of parasites. Nevertheless, this study focused on extraradical mycelium, because no studies have addressed potential parasitism of the mycelium in the root. In view of these considerations, the authors point to some conditions that must be fulfilled in order to conclusively demonstrate the occurrence of parasitism in AMF. As the rhizosphere is such a complex and interaction-rich environment, parasitism should first be shown to occur in sterile conditions, so that potentially misleading abiotic and biotic factors additionally affecting AMF are eliminated. Using an artificial medium is also an advantage for extraction and direct microscopic observation of the entire AMF biomass, which is usually difficult to achieve by traditional soil-based methods. Focusing initially on a target species of AMF is also advantageous, since otherwise AMF community responses could confound the effects of parasitic attack. When designing experiments under the above conditions, additional attention must be paid to these conditions: (1) ensuring that AMF are alive; otherwise parasites could be confounded with saprobes; (2) the population of potential parasites has to be experimentally added to the AMF population, followed by measurement of its effects compared to a control condition consisting of only AMF (and host plant); (3) the two populations in question must be observed in close contact. However, the sole observation of AMF intracellular organisms does not constitute proof of parasitism, as is sometimes implicitly assumed. Subsequent to fulfilling these criteria, the same relationship must be found in situ, in order to ensure that observations made under controlled conditions have ecological meaning and applicability. This is a very difficult step, given the complexity of the soil system. However, ideally, the parasite experiment will have been informed by an observation made in the field or knowledge of typical ‘suspects’ in the first place.

What is the evidence for parasitism of AMF by soil biota? Parasitism of AMF by fungi Parasites of fungi can be divided into two groups, namely biotrophs (the host fungus remains alive) and necrotrophs (parasitism results in death of the host fungus). They may exhibit different host–parasite interfaces ranging from close contact to complete hyphal disruption (Jeffries, 1995). Some 2007 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved

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visual evidence of parasitism is coiling of parasitic hyphae around host hyphae, physical damage and lysis of host hyphal walls, and disruption of cell organelles (Dix & Webster, 1995). These are pieces of evidence more related to necrotrophic parasites, and exemplify a more aggressive situation that culminates in the death of the host, instead of merely reducing fitness. On the other hand, the formation of stable interfaces seems to be more common in biotrophic parasitism, where absorption of nutrients does not lead to host death. The formation of specialized hyphae (i.e. haustorium) during invasion of host mycelium is an example of common evidence of these interfaces (reviewed by Jeffries, 1995). Even though evidence from the fossil record indicates that parasitism in fungi is an evolutionarily old mode of interaction (Hass et al., 1994), there are only a few reports suggesting parasitism of AMF, which are an ancient clade, by other fungi. However, most of these papers merely describe the intracellular occurrence of fungi without making reference to their effects on any fitness parameter (Table 1); this does not constitute unequivocal evidence for parasitism. Some authors carried on more detailed studies, and have tried to measure the influence of fungal invasion on some AMF fitness parameters. Sylvia & Schenck (1983) showed that spores harboring chytrids exhibited reduced germination, whereas root colonization and sporulation by the mycorrhizal fungus were unaffected. On the other hand, Paulitz & Menge (1984) inoculated Gigaspora margarita spores with chytrids (Spizellomyces punctatum) and found no effect on overall spore germination or intraradical hyphae. These conflicting results may be related to compatibility between the (potential) parasite and the host, and also

environmental conditions. However, in the study by Sylvia and Schenck, no distinction was made between alive and dead spores, which would be necessary to show the parasitic nature of the relationship (as opposed to a saprobic interaction). Chytrids seem to establish preferentially in dead spores (100%) compared with live spores (5.6%; Paulitz & Menge, 1984), and it would change the condition of possible biotrophic parasitism to saprotrophism.

Parasitism of AMF by bacteria Most studies regarding bacteria populations associated with AMF focus on isolating bacteria and examining their effects on root pathogens or benefits to plant growth (e.g. Budi et al., 1999; Artursson & Jansson, 2003). Unfortunately, only a few attempts have been made to address the question of the role of bacteria in fitness of mycorrhizal-fungi populations. One example is an interesting study carried out by Xavier & Germida (2003), who measured the effects of AMF surface-associated bacteria on spore germination, mycorrhizal colonization, and plant biomass. Different bacterial species as well as isolates of the same species were found to have a wide range of effects on Glomus clarum. In some situations, evidence of antagonism seemed to be predominant, while in others, facilitation was likely to occur. The authors suggested that this AMF species may synthesize substances that make spores more or less susceptible to parasitic invasion, an idea that needs to be tested. Conversely, most studies report on AMF that just harbor intracellular bacteria, detected either by microscopical observation or by molecular probing (Table 1), which mirrors the questions about the nature of the association already

Table 1. Fulfillment of parasitism criteria (see text) in various studies dealing with AMF and suspected cases of parasitism Criteria/references

Rousseau et al. (1996)

Ross & Ruttencutter (1977)

Daniels & Menge (1980)

Lee & Koske (1994)

Boyetchko & Tewari (1991)

Experiment in sterile conditions

Yes, with root organ cultures

Yes, using ‘parasite’ isolated from soil

Yes, using ‘parasite’ isolated from soil

No

Single populations of AMF used

Glomus intraradices Yes

Glomus epigaeus and Glomus fasciculatus No

Glomus dimorphicum

Organisms shown to be alive at start of experiment Parasites were experimentally introduced to AMF population

Glomus macrocarpus and Gigaspora gigantea No

Yes, using ‘parasite’ isolated from AMF spores Gigaspora gigantea Yes

No

Yes – Trichoderma harzianum

Yes – ‘Pythium-like’ fungus

Yes – 31 isolates

No

Yes No

Yes No

Yes – Acaulospora pseudolongissima and H. fuscoatra Yes No

Yes No

Yes No

None

None

None

None

None

Close contact observed Fitness parameter measured for both populations Follow-up observation in soil environment confirming loss of AMF fitness.

In none of the cases has parasitism been conclusively demonstrated. No data are available yet on viral associations.

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raised for mycoparasites. Could these bacteria have an effect on fungal growth and functionality, or are they found in mycorrhizal structures without implying detrimental consequences? As already mentioned, close contact between organisms is essential to characterize parasitism, but it does not define the ultimate relationship by itself. The fact that some AMF may even favor invasion of spores by some bacteria that increase spore germination (Mayo et al., 1986; Levy et al., 2003) is a very strong argument against suggesting parasitism based only on visual observations. These problems are not exclusive to AMF; bacterial parasitism is poorly understood in other groups of fungi. One exception is the study conducted by De Boer et al. (2001), where the authors isolated bacterial strains from dune soils; these were experimentally added to three filamentous fungi (Chaetomium globosum, Fusarium culmorum, and Mucor hiemalis) under sterile controlled conditions. They observed that Collimonas fungivorans bacteria were able to lyse fungal mycelium and use living hyphae as growth substrate, leading to a significant increase in the size of the bacterial population. This report of parasitism in filamentous fungi thus represents a template for testing this relationship in AMF.

Parasitism of AMF by viruses Another group to be considered in association with AMF is viruses. Fungal viruses in general are not known to have an extracellular phase in their life cycles, and are thought to be transmitted during cell division, fusion, or spore formation, mechanisms that imply limited host compatibility (Ghabrial, 1998). Unfortunately, there is only a single study about the occurrence of virus-like particles in AMF mycelium, in spores of Scutellospora castanea (Hijri et al., 2002). The particles were observed by transmission electron microscopy when the authors were focusing on intracellular bacteria, but no further effort was devoted to confirm the nature of the particles or the significance of this observation. To the authors knowledge, there is no report yet on the functional consequences of viruses in the mycelium. This lack of reports about AMF viruses may be due to the paucity of studies devoted to their detection and difficulties associated with viral identification, but may also be due to a low or null occurrence of viruses in AMF. If the latter is true, why does null occurrence happen? Because initial infection occurs, but without lasting fungal/viral compatibility, or because the mycelium is somehow defended against viral infection? Recent studies have shown that there is a role for viruses in regulating the growth and metabolism of diverse pathogenic and mutualistic fungi (Rogers et al., 1986; Zabalgogeazcoa et al., 1998). Indeed, sometimes viral infection is mandatory for fungal benefits to host plants (Ma´ rquez et al., 2007). Such intimate interactions represent evidence of host dependence FEMS Microbiol Lett 279 (2008) 8–14

for growth and reproduction; hence, the occurrence and significance of viruses in AMF and its possible parasitic nature deserve research attention.

AMF defense strategies against parasites? The literature reviewed suggested that parasitism occurs in AMF, but according to the authors’ criteria, there is no clear evidence yet of necrotrophic or biotrophic parasitism in AMF, despite the widespread occurrence of this interaction in other filamentous fungi. This observation could be due to the rather limited number of studies devoted to this topic (Table 1). An alternative view is that AMF are not highly susceptible to parasites. If that is so, what advantageous trait(s) could AMF have gained that confers apparent resistance to parasites in a high-level interactive environment like the rhizosphere? Mycorrhizal fungal spores have a high content of lipid globules (Maia & Kimbrough, 1998), and there is no real evidence of parasitism in these structures, as well as in hyphae, which represent an active transport of nutrients. It has been suggested that spores exude substances that act as repellants, and as a consequence fungi would not grow on healthy AMF spores (Paulitz & Menge, 1984). However, this hypothesis remains to be tested. In addition to the secretion of substances, another factor that is likely to be involved in AMF resistance to parasitism is the melanin content of the spores. It has been shown that white or lightcolored spores like Gigaspora margarita are more susceptible to harboring bacteria than dark-colored spores of Glomus constrictum (Schenck & Nicholson, 1977; Sneh et al., 1977). Also spores of the same species (Glomus epigaeus) are more resistant to other organisms at maturity, following melanization (Sneh et al., 1977). However, care must be taken in the interpretation of studies of this nature if they were conducted under laboratory conditions. Melanin production is sometimes a result of media nutrient levels (Butler & Lachance, 1987), and therefore results are potentially not applicable to soil environments. It has also been suggested that glomalin, a putative heat shock protein (Hsp 60) homolog produced by AMF, may confer resistance against parasitism (Purin & Rillig, 2007). In fact, some Hsp homologues are related to toxicity and organism resistance to pathogenic bacteria (Yoshida et al., 2001; Sung et al., 2007). However, the hypothesis of glomalin being involved in AMF defense against parasites still remains to be experimentally tested.

What would be the consequences of AMF parasitism at an ecosystem scale? If AMF are parasitized, it must imply decrease of their fitness, however measured. It seems likely that the fungi will 2007 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved

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try to compensate for the lack of metabolites or repair the damaged tissue, requiring increased nutrient uptake from either soil or plant. As a consequence, the flow of photosynthates from plant to the fungus may be higher than when AMF are not parasitized. In this situation, mycorrhizal fungi may change from mutualistic to parasitic symbionts of plants, a condition that causes reduction of plant growth and yield (Klironomos, 2003; Lendzemo et al., 2004). Another possible scenario is the occurrence of parasites when AMF themselves behave like parasites of plants instead of mutualists. In this case parasitism of AMF might shift the mycorrhizal symbiosis even further towards parasitism. If only some AMF species in a resident community suffer a fitness reduction due to parasitism, this could lead to the relative predominance of AMF species with greater resistance, i.e. parasitism could contribute to structuring AMF communities. However, changes in AMF identity or community composition are known to have consequences for plant growth (e.g. Streitwolf-Engel et al., 1997; Maherali & Klironomos, 2007), plant community composition, and ecosystem-level processes (e.g. van der Heijden et al., 1998; Piotrowski et al., 2004). Parasitism could also have implications in a more applied context. AMF are utilized to increase the success of restoration in degraded lands (Cuenca et al., 1998; Requena et al., 2001), AMF inocula can be used as bio-‘fertilizers’, and are considered as biocontrol agents, attacking plant pathogens in agricultural systems (Habte et al., 1999; Kahiluoto et al., 2001). Because of that, AMF inoculum production is a growing worldwide industry (Schwartz et al., 2006); however, the dimension of parasitic effects on inoculum biomass or effectiveness is poorly understood. The occurrence of a parasite in any of these applied situations would contribute to a reduced AMF benefit, with considerable economic consequences. Another important consideration relates to parasites that are used for the biocontrol of fungal plant pathogens. Extensive literature has reported that fungi such as Fusarium and Trichoderma reduce the fitness of plant pathogenic fungi (Larkin & Fravel, 1999; Narisawa et al., 2002), and as a result attenuate plant disease. However, if fungi that are used in biocontrol also have nontarget effects on AMF, this phenomenon would result in a disadvantage for the host plant due to decreased mycorrhizal efficiency. The few studies published on this topic do not provide any evidence for this to occur (Paulitz & Linderman, 1991; Calvet et al., 1993); however, no conclusive statements are yet possible based only on the small number of fungi that have been studied so far.

Final considerations It is evident that parasitism in AMF has not been extensively explored; this study has presented a rationale for this aspect 2007 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved

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S. Purin & M.C. Rillig

of AMF ecology . The authors advise caution with the use of the term parasitism in relation to AMF until unequivocal evidence of such an interaction has been observed. However, the hypothesis that populations of AMF parasites exist introduces a new level of complexity in mycorrhizal associations. This represents an exciting aspect of mycorrhizal ecology that might have diverse consequences for fungal populations and communities, with potentially important effects for plants and ecosystems, including some with an applied relevance. Parasitism might help to explain occurrences such as fungal culture failures or lack of success in applying AMF in the field.

Acknowledgements S.P. was supported by a doctoral fellowship from CAPES (Brazil)/Fulbright. M.C.R. thanks Freie Universit¨at Berlin for support.

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