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The Most Heat‐Resistant Conidia Observed to Date Are Formed By Environmental Microbiology (2020) 22(3), 986–999 doi:10.1111/1462-2920.14791 The most heat-resistant conidia observed to date are formed by distinct strains of Paecilomyces variotii Tom van den Brule,1,2 Maarten Punt,1,3 Introduction Wieke Teertstra,1,3 Jos Houbraken,1,2 Han Wösten 1,3 Fungi produce numerous spores that are distributed by and Jan Dijksterhuis 1,2* water, air and other vectors (as insects, soil movements, 1TiFN, P.O. Box 557, 6700 AN, Wageningen, etc.). Airborne spores are present in every cubic meter of The Netherlands. air and cause fungal colonization in all environments. As 2Department of Applied and Industrial Mycology, reviewed recently, conidia vary in several parameters Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, (Dijksterhuis, 2017). For instance, Aspergillus niger con- 3584 CT, Utrecht, The Netherlands. idia of 5 days old showed higher trehalose content com- 3Utrecht University, Molecular Microbiology, pared with spores of younger age (Teertstra et al., 2017). Padualaan 8, 3584 CH, Utrecht, The Netherlands. Conidia of Aspergillus fumigatus showed differences in pigmentation, compatible solute content and oxidative- Summary and heat-resistance, dependent on the growth tempera- ture of the conidia-forming colony (Hagiwara et al., Fungi colonize habitats by means of spores. These 2017). In general, spore parameters are influenced by cells are stress-resistant compared with growing fun- gal cells. Fungal conidia, asexual spores, formed by conditions during spore formation and maturation. How- cosmopolitan fungal genera like Penicillium, Asper- ever, there is a scarcity of information on the extent of gillus and Peacilomyces are dispersed by air. They heterogeneity of spore populations, even if they origi- are present in places where food products are stored nate from one colony. Stress resistance of spores and and as a result, they cause food spoilage. Here, we germination properties are both important for coloniza- determined the heterogeneity of heat resistance of tion but different in nature. Colonies from individual conidia between and within strains of Paecilomyces spores that enter a new ecosystem often have longer variotii, a spoiler of foods such as margarine, fruit lag times compared with a population of spores juices, canned fruits and non-carbonized sodas. Out (Gougouli and Koutsoumanis, 2013; Dagnas et al., of 108 strains, 31 isolates showed a conidial survival 2015). This is essentially caused by the phenomenon >10% after a 10-min-heat treatment at 59C. Three that the spore that germinates fastest determines the strains with different conidial heat resistance were lag time of a population. Furthermore, germination of selected for further phenotyping. Conidia of DTO 212-C5 conidia is delayed markedly when conditions are sub- and DTO 032-I3 showed 0.3% and 2.6% survival in the optimal. In several studies, this is tested in the case of screening respectively, while survival of DTO 217-A2 water activity and temperature (Dagnas et al., 2017; conidia was >10%. The decimal reduction times of these Nguyen Van Long et al., 2017; Stevenson et al., 2017). strains at 60 C(D60 value) were 3.7 Æ 0.08, 5.5 Æ 0.35 Heterogeneity encountered in conidia is relevant in the and 22.9 Æ 2.00 min respectively. Further in-depth analy- area of food spoilage; the strongest spore will define if sis revealed that the three strains showed differences in spoilage occurs. In nature, the strongest spore enlarges morphology, spore size distributions, compatible solute the limits of growth of a species. Fungal spoilage of compositions and growth under salt stress. Conidia of processed foods and drinks causes food waste and eco- DTO 217-A2 are the most heat-resistant reported so far. nomic losses (Gustavsson et al., 2011). In general, indus- The ecological consequences of this heterogeneity of try prevents fungal food spoilage in their products by resistance, including food spoilage, are discussed. using preservation hurdles like pasteurization, lowering water activity, lowering pH or decrease storage tempera- ture. Consumer demands towards more natural and pre- servative free food put a pressure on shelf life of food Received 15 April, 2019; revised 22 August, 2019; accepted 22 August, 2019. *For correspondence. E-mail j.dijksterhuis@wi. (Leyva Salas et al., 2017). For instance, lowering heat knaw.nl. Tel. (+31) (0)30 2122654; Fax (+31) (0)30 2122601. treatments could lead to more beneficial organoleptic © 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Stress resistance of conidia in fungal strains 987 characteristics of the product and better retainment of results to reflect on the heterogeneity within and between vitamins or other temperature-sensitive healthy compo- the various P. variotii strains. nents. On the other hand, this procedure would introduce survival of heat-resistant cells and more risk for the prod- uct to be spoiled. In addition, consumers demand health- Results ier alternatives, including products containing lower salt Screening conidia for heat resistance concentrations and less use of antimicrobial compounds. These trends towards milder processing methods make In total, 108 P. variotii isolates were used in this study. The processed food products more prone to microbial spoil- strains were isolated from various substrates and locations, age and put a tension on the microbial safety limits of of which most originated from United States or The Nether- processed foods and drinks. lands (Table 1). Of the 108 strains, 65 were isolated from Paecilomyces variotii is a common thermo-tolerant fun- food products or industry environment, 27 originated from gus that occurs worldwide and has been isolated from indoor and outdoor environments and 16 were medical iso- food products, soil samples, clinical samples and indoor lates from human patients or hospital environment. All fi β environments (Houbraken et al., 2010). Recently, the strains were identi ed by DNA sequencing of the -tubulin genomes of P. variotii type strain CBS 101075 and CBS locus (Samson et al., 2009). A maximum likelihood tree rev- 144490 were sequenced (Urquhart et al., 2018). ealed that all P. variotii strains grouped together and were P. variotii produces conidia abundantly and to lesser separated from Paecilomyces brunneolus the closest extent chlamydospores. Besides these spore types, it is related species, with a bootstrap value of 100% (Fig. 1). fi fi also known to produce highly heat-resistant ascospores More intraspeci c clades were identi ed than described in a heterothallic manner (Houbraken et al., 2008). Due before (Houbraken et al., 2008). However, most of these to the resistant nature of these spores and its ability to clades showed bootstrap values below 70%. Within the grow at low oxygen concentrations, it is able to spoil pas- P. variotii group, the overall mean distance was Æ teurized food products like fruit juices, canned fruits and 0.013 0.003 substitutions per site, indicating a low varia- non-carbonized sodas (Pitt and Hocking, 2009). Although tion between the strains. Like recently described, the β P. variotii is a major spoilage fungus in a certain product -tubulin gene from the draft genome of the previously mis- fi niche, many aspects remain elusive in the resistance of identi ed Paecilomyces formosus No5 as P. variotii, groups its propagules. with the type strain of P. formosus inthetree(Okaet al., Compatible solutes like trehalose, mannitol, glycerol, 2014; Urquhart et al., 2018). erythritol and arabitol are accumulated in fungal spores In order to study the variation of heat resistance of con- (Wyatt et al., 2013). Due to the kosmotropic nature of idia among the different strains, conidia of each strain these compounds, they protect cells against various were heat-inactivated in a water bath at 58 or 59 C dur- stressors (Cray et al., 2013). Kosmotropic solutes have ing 10 min. Subsequently, conidia survival was deter- 3 typically a larger affinity to form hydrogen bonds with mined by inoculating 10 conidia on malt extract agar water than water molecules with themselves, resulting in (MEA). After 3 days incubation at 25 C, the number of a stabilizing effect on biomacromolecules like proteins colonies was counted. For 31 isolates, more than 10% of (Washabaugh and Collins, 1986; Collins, 1997). It is the conidia survived the 59 C heat treatment and showed thought that trehalose plays an important role in the heat more than 100 colonies on plates (Fig. S1). The resistance of fungal spores (Wyatt et al., 2013, 2015). A remaining 77 strains showed a broad variety in the num- decrease in trehalose concentration in Aspergillus ber of colonies, stretching from 1 to 94. After the 10 min- nidulans and Aspergillus oryzae conidia resulted in a heat treatment at 58 C, 68 isolates showed more than higher sensitivity to heat stress (Fillinger et al., 2001; 100 colonies after the treatment, while 40 strains showed Sakamoto et al., 2008). between 13 and 95 colonies. Based on sequences of marker genes, P. variotii showed a higher genetic variability than related members In-depth analysis of three strains of the Eurotiales (Houbraken et al., 2008). In this research, we used the conidia of P. variotii as a model to Three strains, DTO 032-I3, DTO 212-C5 and DTO explore the limits and variability of resistance to heat 217-A2 were selected for an in-depth analysis in conidial stress. We used 108 isolates from various substrates and heat resistance, morphology and compatible solute com- locations to screen the conidia for heat resistance. Sub- position. Based on the screening, conidia from strain sequently, we did an in-depth analysis of three strains DTO 032-I3 were rather sensitive, showing 70 and 26 col- of interest in their heat resistance, morphology and com- onies after heat treatment at 58 and 59C respectively.
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