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Dung-Inhabiting Fungi: a Potential Reservoir of Novel Secondary

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Dung-Inhabiting Fungi: a Potential Reservoir of Novel Secondary Review Received: 1 October 2015 Revised: 19 November 2015 Accepted article published: 10 December 2015 Published online in Wiley Online Library: 25 January 2016 (wileyonlinelibrary.com) DOI 10.1002/ps.4206 Dung-inhabiting fungi: a potential reservoir of novel secondary metabolites for the control of plant pathogens Sabrina Sarrocco* Abstract Coprophilous fungi are a large group of saprotrophic fungi mostly found in herbivore dung. The number of these fungi undergoing investigation is continually increasing, and new species and genera continue to be described. Dung-inhabiting fungi play an important ecological role in decomposing and recycling nutrients from animal dung. They produce a large array of bioactive secondary metabolites and have a potent enzymatic arsenal able to utilise even complex molecules. Bioactive secondary metabolites are actively involved in interaction with and defence against other organisms whose growth can be inhibited, resulting in an enhanced ecological fitness of producer strains. Currently, these antibiotics and bioactive secondary metabolites are of interest in medicine in particular, while very little information is available concerning their potential use in agriculture. This review introduces the ecology of dung-inhabiting fungi, with particular emphasis on the production of antibiotic compounds as a means to compete with other microorganisms. Owing to the fast pace of technological progress, new approaches to predicting the biosynthesis of bioactive metabolites are proposed. Coprophilous fungi should be considered as elite candidate organisms for the discovery of novel antifungal compounds, above all in view of their exploitation for crop protection. © 2015 Society of Chemical Industry Keywords: coprophilous fungi; bioactive metabolites; antifungal; plant pathogens; crop protection 1 INTRODUCTION TO THE ECOLOGY OF physical structure, mainly consisting of small fragments within a DUNG-INHABITING FUNGI mucilaginous – but aerated – matrix, makes this medium suitable for fungal growth.7,8 Fungi play a major role within the complex The term ‘coprophilous’ is generally used to describe fungi that biota responsible for dung decomposition, as it would seem that inhabit dung. Many species are exclusive to dung, whereas others, they are the principal users of faecal cellulose and lignin, produc- although most common on faeces, can survive on other types of ing biomass that is later used by other microorganisms, and con- decaying organic matter.1 ditioning the substrate so that it becomes a favourable habitat for Doveri2 prefaced his book Fungi Fimicoli Italici describing the a variety of invertebrates.9 origins of the term coprophilous and its applicability. The same meaning of the term coprophilous has often been assigned to fimicolous.3,4 As explained by Barrasa,5 the two words contain 1.1 Fungal succession on dung ‘copros’ (from Greek) and ‘fimus’ (from Latin), both meaning dung. Facing a highly competitive pressure for space in order to produce Doveri elegantly highlighted how the slight difference consists in their fruit bodies on the dung surface, a temporal and taxonomic the meaning of the suffixes – philous (from the Greek ‘I love’) and succession partially explains the order of appearance of these 10 – 12 colous (from the Latin ‘I live’ or also ‘I frequent a place’), which fungi on dung. Several works have described the sequence suggests using coprophilous to define all fungi obligatorily living of fungal fruiting body formation on dung, many of which have on dung, and to use fimicolous more broadly to refer to those fungi highlighted the fact that the succession follows a taxonomic that optionally live on dung but that are also able to develop on grouping (Zygomycetes, Ascomycetes and Basidiomycetes). In other substrates as well. Hereafter, coprophilous will be used as a this context, the ‘nutritional hypothesis’ has been accepted as synonym of fimicolous, as it is normally the case that authors do a way to correlate the succession to the nutritional require- not specify whether in using such terms they take into account the ments of these groups of fungi for spore germination, mycelial different meanings of the two suffixes. growth and reproductive structures. According to this hypothe- From an ecological point of view, animal dung represents a rich sis, Zygomycetes such as Pilobolus, Circinella and Cunninghamella medium for fungal growth. It contains a high amount of read- ily available carbohydrates (including hemicellulose, cellulose or lignin) and a high nitrogen content. Herbivorous dung can contain ∗ Correspondence to: S Sarrocco, Department of Agriculture, Food and Environ- 4% nitrogen, which is more than the plant material originally eaten ment, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy. E-mail: [email protected] by animals.6 It also contains vitamins, growth factors and minerals, 643 in addition to a high amount of water and a pH of around 6.5. Its Department of Agriculture, Food and Environment, University of Pisa, Pisa, Italy Pest Manag Sci 2016; 72: 643–652 www.soci.org © 2015 Society of Chemical Industry www.soci.org S Sarrocco are the first to appear owing to their ability to metabolise fairly and Cooke21 observed a reduction in the number of ascocarps accessible carbon sources, such as sugars. Their growth rate is when more than one species was present, with Ascobolus crenu- rapid, and they disappear as soon as this substrate is exhausted latus being particularly sensitive to cohabitation together with and are succeeded by Ascomycetes, including Sordaria, Podospora, Chaetomium bostrycodes and Sordaria macrospora. The conclusion Arthrobotrys or Trichurus. These, the second actors in order of was that the observed reduction in fruiting bodies was due to appearance in this scenario, are able to degrade complex car- competition for nutrients in the absence of evidence of combative bon sources such as cellulose and hemicellulose. Finally, dung competition, with a higher decomposition rate when substrates is colonised by Basidiomycetes, mainly Coprinus and Coprinellus were inoculated by more than one fungus. species,13 which appear last but persist longer, as they exploit not Antagonistic interactions between two or more coprophilous only cellulose but also the complex lignin. fungi can occur either at a distance or upon/after physical contact Given that this nutritional hypothesis may not be sufficient to between individual hyphae or mycelial networks.22 Active recog- explain all aspects of dung colonisation, a second hypothesis has nition of the presence of other mycelia is required and represents been advanced, based on the time it takes for each fungus to accu- the beginning of a combative response, although, in some cases, mulate enough nutritional reserves to enable it to fruit.6 The suc- contact between individual hyphae must occur before a response cession Zygomycota–Ascomycota–Basidiomycota supports this is stimulated, sometimes followed by cell death at one or both hypothesis, as it is evident that simple sporangiophores need mycelial fronts.19 fewer nutrients and a shorter time to develop than the fruiting Hyphal interference involves contact between an antagonist and bodies of Ascomycetes or the larger basidiomata which require a sensitive fungus. The resolution of this kind of interaction is the more time to be differentiated. lysis of those cells of the sensitive fungus in contact with the antag- In addition to this temporal hypothesis, one more factor, inter- onist and the final death of the prey. The involvement of hyphal specific competition (that is, an interplay of biological, physical interference within the dung fungal succession is well known. In and nutritional factors), has been suggested as a complemen- 1964, Harper and Webster23 observed that the fruiting of Pilaira tary explanation for both the nutritional and reproduction time anomala and Ascobolus crenulatus was reduced when Coprinus 2,12,14 hypotheses in explaining fungal succession on dung. Inter- heptemerus spores were added in a mixed spore suspension. specific competition between fungi on dung has been histori- In 1970, Ikediugwu and Webster24 tested a range of coprophilous cally described as the result of many forms of interaction, such and non-coprophilous fungi in terms of their ability to cause as competition for nutrients, hyphal interference, including myco- hyphal interference and their sensitivity to it. They reported that 1 parasitism, and the production of antibiotics. Cooke and Rayner Coprinus heptemerus led to depression and premature cessation defined competition as ‘an active demand by two or more individ- of the fruiting of two coprophilous fungi (Pilobolus crystallinus uals of the same or different species for the same resource’, imply- and Ascobolus crenulatus), which was also observed in all the ing the active demand for nutrients, oxygen, water and space. basidiomycetes that they tested. The effect of Coprinus against Competition can take the form of primary resource capture or com- Ascobolus was evident only after contact between the two fungi, bat. Capture is when a fungus gains access to a resource by a rapid with a dramatic change in the condition of Ascobolus hyphae, spore germination and mycelial growth rate, achieved by versa- which stopped growing, developed refractile walls and vacuo- tile enzyme production. Combat describes the defence of the cap- lated contents and lost turgor, but no production of diffusible tured territory (substrate), or the strategy of seizing
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