Skip to main content

Combined effect of water activity and pH on the growth of food-related ascospore-forming molds

Abstract

Purpose

The contamination of raw materials, packaging, or processing environments by fungal ascospores is a real concern for food industries, where variable rates of spoilage can be reached in pasteurized acidic products such as fruit juices, fruit jams, or soft drinks. The aim of this work was to assess the combined effect of aw and pH on the growth of six isolates from three genera of ascospore-forming molds that may occur in raw materials and in food industrial environments, in order to determine the environmental conditions that prevent the spoilage of pasteurized foods and beverages.

Methods

Growth tests were carried out on 60-day-old ascospores from Aspergillus hiratsukae (≡Neosartorya hiratsukae), Aspergillus thermomutatus (≡Neosartorya pseudofischeri), Chaetomium flavoviride, Chaetomium globosum, Talaromyces bacillisporus, and Talaromyces trachyspermus. The tests were performed up to 90 days at 25 °C, using sucrose solutions at different aw (0.85, 0.88, 0.92, 0.95) and pH (3.20, 3.50, 3.80, 4.20, 4.60) values. Growth was characterized by fitting an ordinary logistic regression model to the collected growth data.

Results

The explained percentage of the growth/no growth models ranged between 81.0 and 99.3%: aw exerted the largest influence on the growth of all tested species, while pH was significant only for Chaetomium isolates. The minimum conditions for germination and growth were aw 0.92 and pH 3.50 or 3.80, respectively, for C. flavoviride (46 days) and C. globosum (39 days), aw 0.92 and pH 3.20 for T. trachyspermus (13 days), aw 0.88 and pH 3.20 for T. bacillisporus (39 days), and aw 0.88 and pH 3.20 for the two aspergilli (33 and 27 days, respectively, for A. hiratsukae and A. thermomutatus).

Conclusions

Most of the spoiling mycetes tested were well-adapted to the formulations considered; therefore, foods strategies aiming to inhibit their growth should explore also the hurdle effect exerted by other factors (e.g., antioxidants, organic acids, oxygen levels).

Introduction

About one third of the food produced for human consumption every year is lost or wasted (EU 2016; FAO 2012). Although losses due to microbial contamination or spoilage by bacteria, yeasts, and molds are not well-documented, this is a real concern for the food industry (Elkhishin et al. 2017). For pasteurized high acidic fruit products, where only some microorganisms can grow, most of the juice processor members from the American Juice Products Association (JPA) and the European International Fruit and Vegetable Juice Association (IFU) declared to be forced to discard ingredients or product at least once a year due to microbial spoilage, and that the presence of Alicyclobacillus species or Heat-Resistant Molds (HRM) is a serious threat to food quality, so much that 64% of them have experienced HRM spoilage of finished products (Snyder and Worobo 2018). Among the abovementioned microorganisms, HRM can be considered more adaptable than alicyclobacilli because they grow across a wider range of temperature and pH, as well as at minimal oxygen headspace concentrations (dos Santos et al. 2020; Pitt and Hocking 2009; Samson et al. 2010). This means that, once ascospores are activated by pasteurization treatments, their germination and growth can hardly be hindered, leading to relevant incidental spoilage cases (Rico-Munoz 2017). Apart from accurate monitoring of ingredients, processing environments and packaging, most of the industrial processing steps do not significantly reduce ascospores presence (dos Santos et al. 2018); additionally, the use of preservatives such as sorbate, benzoate, and sulfur dioxide (King et al. 1969) or of technological aids such as chitosan (Manusia and Berni 2017) proved only partially effective or completely ineffective against HRM.

To prevent or limit contamination, acting on physico-chemical parameters such as water activity (aw), hydrogen ion concentration (pH), or dissolved oxygen levels can achieve the so-called “hurdle-effect”. Unfortunately, the literature data concerning this topic are limited to only a few fungal species: the aw influence on ascospore germination and growth was studied on Byssochlamys species (Panagou et al. 2010; Roland and Beuchat 1984; Valík and Piecková 2001), Neosartorya fischeri (Valík and Piecková 2001; Zimmermann et al. 2011), Eurotium species (Greco et al. 2018), or Talaromyces avellaneus (Valík and Piecková 2001); the effect of oxygen levels was investigated on Byssochlamys species by Taniwaki et al. (2001) and on Byssochlamys and Neosartorya isolates by dos Santos et al. (2019). The combined influence of different parameters on ascospore-forming species was explored only on Monascus ruber (Panagou et al. 2003) and Neosartorya fischeri (dos Santos et al. 2020; Nielsen et al. 1988; Nielsen 1991).

Therefore, the aim of this work was to assess the combined effect of aw and pH on the growth of isolates from three different genera of ascospore-forming molds (Aspergillus with Neosartorya morphs; Talaromyces; Chaetomium) commonly detected in raw materials and in industrial environments (dos Santos et al. 2018; Rico-Munoz and dos Santos 2019; Sato and Takei 2000; Tranquillini et al. 2017), in order to find the best conditions to avoid fungal spoilage of pasteurized foods and beverages.

Materials and methods

Microorganisms

This study was carried out using the following fungal strains:

  • Aspergillus hiratsukae (≡ Neosartorya hiratsukae) SSICA 3913, isolated from a spoiled tea beverage

  • Aspergillus thermomutatus (≡Neosartorya pseudofischeri) SSICA 121014, isolated from spoiled strawberry jam

  • Chaetomium globosum DSM 1962, isolated from stored cotton in the USA

  • Chaetomium flavoviride ATCC 32404, isolated from dead Juncus stems in Hungary

  • Talaromyces bacillisporus SSICA 10915, isolated from heat-treated blueberries

  • Talaromyces trachyspermus SSICA 15007, isolated from heat-treated berries

Talaromyces and Aspergillus were tested because their presence in raw materials used for food and beverage production is well known. Chaetomium were assessed because they are resistant to the chemical agents used for sanitation of industrial food plants (Scaramuzza et al. 2020a; Scaramuzza et al. 2020b) and are responsible for spoilage in foods packaged by aseptic filling machines (Sato and Takano 2000).

Preparation of ascospore suspensions

Ascospore suspensions were prepared according to Scaramuzza et al. (2020a). Briefly, each isolate was purified, spread on potato dextrose agar (PDA, Oxoid, Cambridge, UK) in Petri dishes, and incubated at 30 °C up to 60 days to enhance ascospore production and to increase resistance (Conner and Beuchat 1987; Dijksterhuis and Teunissen 2004; King and Whitehand 1990; Tournas and Traxler 1994). Mycelium and ascomata were collected into a sterile glass bottle containing a 0.1% (v/v) Tween 80 solution and sterile glass beads (3 mm diameter), shaken for 5 min using a mixer (Vortex, Continental Instruments), and filtered through sterile glass wool. Spore concentration was assessed by means of a differential interference contrast (DIC) microscope (Eclipse 80i, Nikon, Tokyo, Japan), to confirm that each was a suspension with free ascospores. Filtered spores suspensions were stored at − 20 °C until use.

Growth tests

All tests were carried out using sucrose solutions to attain a wide range of aw values (0.85–0.95). Sucrose solutions, prepared according to Grover and Nicol (1940), at aw 0.85, 0.88, 0.92, and 0.95 showed 65.6, 61.0, 51.4, and 39.8 °Bx, respectively. All solutions were sterilized at 115 °C for 10 min, and their pH was aseptically adjusted with 5.0% citric acid to obtain pH values equal to 3.20, 3.50, 3.80, 4.20, and 4.60.

The aw was measured using an aw meter (LabMaster Novasina GmbH, Pfäffikon, Switzerland). The total soluble solids were measured by means of PAL-3 a refractometer (Atago, Tokio, Japan) as degrees Brix that corresponds to 1 g of sucrose in 100 g solution. The pH was measured using a pH meter (Seven Compact S220, Mettler Toledo, Columbus, OH, USA) equipped with an “EasyFerm Bio HB-MS 160” electrode (Hamilton Bonaduz AG, Bonaduz, Switzerland).

Physico-chemical analyses were carried out on uninoculated solutions at the beginning and at the end of the tests, in order to check the maintenance of initial aw, °Bx, and pH.

Each aw-pH combination was transferred into 20-ml Pyrex® round-bottom sterile tubes with screw cap (7 ml per tube, in order to keep a sufficient headspace) and separately inoculated with 0.05 ml of each ascospore suspension. These tubes permit a homogeneous distribution of the inoculated spores in the solution by means of a vortex apparatus, whereas screw caps allow to maintain sterility without altering the composition of the inoculated medium during the test. Chaetomium suspensions were not heat-treated, since their reproductive structures are heat sensitive, albeit resistant to chemical stresses. On the contrary, Talaromyces and Aspergillus ascospores were heat-treated at sub-lethal temperatures (75 °C) for 30 min, in order to break their dormant state and start the germination (Dijksterhuis 2007). Both inoculated and uninoculated (negative controls) tubes were incubated at 25 °C up to a maximum of 90 days and checked daily to assess the development of hyphal filaments. In case of mycelial growth, the filaments detected were transferred on acidified PDA plates for confirmation. All combinations were tested in triplicate.

Statistical analysis

The results of the growth data at each aw underwent the analysis of variance (ANOVA) considering pH as factor and, when significant, Fisher’s least significant difference tests (LSD) at p ≤ 0.05 were performed. The analyses were done using the statistical program STATGRAPHICS® Centurion. Mean values, standard error, and coefficient of variation were calculated using the Excel program (Microsoft® Office Excel 2016).

Development of growth/no growth models

Growth data were used to develop models for all the fungi tested, with aw, pH, and time of incubation as explanatory variables. A total of 180 data for each isolate (60 combinations of aw, pH, and time with three replicates) was considered for the construction of each model. An ordinary logistic regression model (Gysemans et al. 2007) consisting of a polynomial (right-hand side) and \( \mathrm{logit}\ (p)=\ln \frac{p}{\left(1-p\right)} \) (left-hand side), where logit is the logistic unit and p is the probability that growth occurs (0 ≤ p ≤ 1), was used to describe the data. The logistic regression model (below) included the main factors; their interactions and the quadratic expression of main factors, bi (i = 0,…, 8) are the parameters to be estimated:

$$ \mathrm{logit}\ (p)={b}_0+{b}_1{a}_w+{b}_2\ \mathrm{pH}+{b}_3\ \mathrm{time}+{b}_4{a}_w\mathrm{pH}+{b}_5{a}_w\ \mathrm{time}+{b}_5\ \mathrm{pH}\ \mathrm{time}+{b}_6\ {a_w}^2+{b}_7\ {\mathrm{pH}}^2+{b}_8\ {\mathrm{time}}^2 $$

The models were fitted with the statistical program STATGRAPHICS® Centurion; the terms were selected by the forward stepwise procedure, based on the significance of the likelihood-ratio criterion (p < 0.001).

Results

High acidic foods are usually heat-treated and stored at room temperature; in order to mimic the commercial life of such products, our tests were therefore carried out at 25 °C. Furthermore, in high acidic products, the real concern for food industries is the visible spoilage by fungal mycelium that unavoidably leads to consumer rejection; thus, the tests were focused on mycelial growth rather than on ascospores germination. In this study, the fungal growth was tested in sucrose solutions under different conditions.

The growing ability of six fungal isolates was studied under combinations of four aw (0.85, 0.88, 0.92, and 0.95) and five pH values (3.20, 3.50, 3.80, 4.20, and 4.60) at 7, 30, and 90 days of incubation. Figures 1, 2, and 3 show an overview of the results regarding the growth/no growth conditions of the different strains. The estimated parameters (p ≤ 0.001) with their standard errors are summarized in Table 1. The variance explained by the models ranged between 81.0 and 99.3% and the adjusted percentages between 77.8 and 96.7%.

Fig. 1
figure1

Growth/no growth conditions of Chaetomium flavoviride and Chaetomium globosum as a function of aw, pH, and incubation time (7, 30, and 90 days). Solid symbols indicate microbial growth; open symbols indicate no growth

Fig. 2
figure2

Growth/no growth conditions of Talaromyces trachyspermus and Talaromyces bacillisporus as a function of aw, pH, and incubation time (7, 30, and 90 days). Solid symbols indicate microbial growth; open symbols indicate no growth

Fig. 3
figure3

Growth/no growth conditions of Aspergillus hiratsukae (Neosartorya hiratsukae) and Aspergillus thermomutatus (≡Neosartorya pseudofischeri) as a function of aw, pH, and incubation time (7, 30, and 90 days). Solid symbols indicate microbial growth; open symbols indicate no growth

Table 1 Estimated coefficients ± standard errors from the second logistic regression model (p < 0.001)

Among the physico-chemical factors considered, aw exerted the largest influence on the growth of all strains; a significant pH effect was observed only on C. flavoviride and C. globosum growth, where the interaction with incubation time was significant as well (Table 1).

The growth/no growth models concerning Chaetomium strains (Fig. 1) recorded the lowest values for germination and growth at aw 0.92 and pH 3.50 or 3.80, respectively, for C. flavoviride and C. globosum, whereas the highest growth rate was observed for both strains at aw 0.95 and pH down to 4.20. For Talaromyces strains (Fig. 2), a marked interspecific difference was observed: the lowest values for germination and growth were recorded at aw 0.92 and pH 3.20 for T. trachyspermus and at aw 0.88 and pH 3.20 for T. bacillisporus. On the contrary, the highest growth rate occurred at higher aw (0.95) regardless of the pH. For Aspergillus strains within the group Neosartorya (Fig. 3), the minimum aw and pH values for germination and growth were 0.88 and 3.20 for both strains. For such isolates, the fastest growth was observed at aw 0.95, regardless of the pH considered.

The average growth time of the fungi tested in different sucrose solutions is shown in Table 2. The time increase needed for mycelium formation was a function of aw decrease. Specifically, the combined effect of aw and pH mostly induced an increment in the number of days needed for micro-mycelia formation in all the strains tested, when increasing concentrations of sucrose were considered. At high aw values (0.95), the number of days for growth was always not significantly different (p > 0.05) at the various pH and for all tested isolates, except for Chaetomium strains. On the contrary, when lower aw values were tested, the optimum growth conditions greatly differed for each strain and among replicates. At aw 0.88, a first hurdle effect (no growth) was recorded for three out of six tested fungi; at aw 0.85, no strain germinated and consequently did not develop micro-mycelia (Figs. 1, 2, and 3).

Table 2 Growth time (days) ± standard deviation (n = 3) for ascospore-forming molds at various aw and pH values

Discussion

Chaetomium isolates were hydrophilic, i.e., did not germinate and grow at aw < 0.90; furthermore, while at aw 0.95, they were able to grow within 7 days regardless of the pH considered, at aw 0.92 their growth was inhibited if the pH was lower than 3.50. Under this aw-pH combination, the germination time varied from 40 to 52 days for C. flavoviride, whereas C. globosum did not germinate at all. This could be due to the fact that C. globosum has both a hydrophilic and a neutrophilic nature, mainly growing at aw > 0.90 and pH between 4.3 and 9.4 (Pitt and Hocking 2009); only recently it showed reduced growth even at pH 3.51, although an anomalous morphology was observed (Straus 2011).

Talaromyces isolates varied in their xerotolerance. At aw 0.95, the tested isolates grew within 3 (T. bacillisporus) or 6 (T. trachyspermus) days; at lower aw values, both strains showed an inflection point in days needed for growth at pH 3.80 (aw 0.92) or at pH varying from 3.50 to 3.80 (aw 0.88). At the latter aw value, T. bacillisporus was the only strain that produced micro-mycelia at all pH tested in 23–41 days, whereas T. trachyspermus did not grow at all. Our results are hardly comparable with literature results since, to the best of our knowledge, studies concerning lowest aw for germination and growth of Talaromyces species are missing. The only exception is an early study by Hocking and Pitt (1979) where minimum aw values of 0.84, 0.86, 0.88, and 0.90 (14 days at 25 °C) were reported for T. purpurogenus, T. islandicus, T. wortmannii, and T. funicoulosus, respectively. Such data refer to glycerol-based media and conidia, because at that time the abovementioned species were still identified as Penicillium.

Aspergillus isolates with Neosartorya morphs were found the most xerotolerant, with little differences between isolates. At aw 0.95, both A. hiratsukae and A. thermomutatus were able to develop mycelium within 3 or 4 days, respectively. At aw 0.92, growth times of A. hiratsukae varied from 3 to 5 days, whereas those of A. thermomutatus were twice those at 0.95, excepted at pH 3.80. At aw 0.88, the number of days for growth increased from 18 to 33 (A. hiratsukae) and from 22 to 29 (A. thermomutatus) with decreasing pHs. These results are comparable with those obtained by Berni et al. (2017) in strawberry-based media inoculated with Aspergilli showing Neosartorya morphs, where the reported number of days needed for growth were similar at aw 0.92, but no growth was observed on one strain of A. hiratsukae and the same strain of A. thermomutatus, maybe due to the preserving effect exerted by the citric acid present in strawberries that proved able to retard and/or inhibit ascospores growth (Amaeze 2013; Campo and Santos 2006; dos Santos et al. 2019; Sturm et al. 2003). Analogously, our data largely overlap those by dos Santos et al. (2020) which observed a minimum number of days for Neosartorya fischeri growth ranging from 18 to 40 under similar conditions (30 °C; 0.88 aw; 0.8% oxygen levels). On the contrary, Valík and Piecková (2001) reported N. fischeri ability to grow, at reduced rates, even at aw 0.85, the little discrepancy with our study being probably attributable to the different experimental conditions applied.

In general, aw effect proved strain-dependent for Talaromyces and Chaetomium strains that displayed different behaviors when the same physico-chemical conditions were applied. Considering the same pH value, optimal growth always occurred at the highest aw value (0.95) for all tested fungi. On the contrary, the pH influence proved to be genus-dependent: considering the same aw value, mild acid conditions (pH 4.50) were optimal for Chaetomium and Aspergilli with Neosartorya ascospores, whereas lower values (pH 3.80) were optimal for Talaromyces isolates growth. These findings can be considered a confirmation of the fact that aw is one of the dominant environmental factors governing food stability and spoilage by molds, whereas pH usually exerts minor effects over a broad range (3–8) (Pitt and Hocking 2009).

Conclusions

During the last decades, studies concerning the combined effects of different physico-chemical parameters on ascospore-forming species have been sporadically carried out on a limited number of fungal species. Nevertheless, their possible presence in raw materials, packaging, or processing environments is a real concern for food industries, where variable rates of spoilage can be reached in pasteurized acid products such as fruit juices, fruit jams, or sugar-added beverages. Therefore, the search for punctual data and predictive models by food producers is increasing due to the need to avoid microbial-related spoilage incidents and reputation damages. This study was carried out to provide the food industry with a reference point in the early steps of the production process, when target spoilage microorganisms and thermal parameters must be defined.

Our results indicate the optimal and limiting growth conditions for the fungi examined and highlight the synergistic effects between aw and pH in sucrose-added models mimicking acid-pasteurized beverages. Considering the influence of hydrogen ion concentration, the optimal growth conditions for the ascospore-forming molds occurred when pH values were between 3.80 and 4.50, even if values down to 3.20 did not always inhibit or inactivate them, meaning that these mycetes are well-adapted to pH of pasteurized products. Considering the effect of aw, the optimal growth conditions were recorded at the highest value (0.95). Although fungal growth was observed at aw values as low as 0.88 (Talaromyces and Aspergillus with Neosartorya morphs) or 0.92 (Chaetomium), none of the tested isolates proved xerophile, i.e., able to grow below 0.85 in at least one set of tested environmental conditions.

Availability of data and materials

The authors declare that all materials and data are available.

References

  1. Amaeze NJ (2013) Effect of different fruit components, aeration and cold storage at 5 °C on the germination of ascospores of Neosartorya fischeri. Lett Appl Microbiol 56:443–448. https://doi.org/10.1111/lam.12072

    CAS  Article  PubMed  Google Scholar 

  2. Berni E, Tranquillini R, Scaramuzza N, Brutti A, Bernini V (2017) Aspergilli with Neosartorya-type ascospores: heat resistance and effect of sugar concentration on growth and spoilage incidence in berry products. Int J Food Microbiol 258:81–88. https://doi.org/10.1016/j.ijfoodmicro.2017.07.008

    CAS  Article  PubMed  Google Scholar 

  3. Campo G, Santos JI (2006) Quantitative analysis of malic and citric acids in fruit juices using proton nuclear magnetic resonance spectroscopy. Anal Chim Acta 556:462–468. https://doi.org/10.1016/j.aca.2005.09.039

    CAS  Article  Google Scholar 

  4. Conner DR, Beuchat LR (1987) Efficacy of media for promoting ascospore formation by Neosartorya fischeri, and the influence of age and culture temperature on heat resistance of ascospores. Food Microbiol 4:229–238. https://doi.org/10.1016/0740-0020(87)90005-0

    Article  Google Scholar 

  5. Dijksterhuis J (2007) Heat resistant ascospores. In: Dijksterhuis J (ed) Food Mycology. A multifaceted approach to fungi and food. CRC Press, Boca Raton, pp 101–117

    Chapter  Google Scholar 

  6. Dijksterhuis J, Teunissen PGM (2004) Dormant ascospores of Talaromyces macrosporus are activated to germinate after treatment with ultra-high pressure. J Appl Microbiol 96:162–169. https://doi.org/10.1046/j.1365-2672.2003.02133.x

    CAS  Article  PubMed  Google Scholar 

  7. dos Santos JLP, Samapundo S, Biyiklib A, Van Impe J, Akkermans S, Höfte M, Abatihe EN, Sant'Ana AS, Devlieghere F (2018) Occurrence, distribution and contamination levels of heat-resistant moulds throughout the processing of pasteurized high-acid fruit products. Int J Food Microbiol 281:72–81. https://doi.org/10.1016/j.ijfoodmicro.2018.05.019

    CAS  Article  PubMed  Google Scholar 

  8. dos Santos JLP, Samapundo S, Cadore Pimentel G, Van Impe J, Sant’Ana AS, Devlieghere F (2019) Assessment of minimum oxygen concentrations for the growth of heat-resistant moulds. Food Microbiol 84:103243. https://doi.org/10.1016/j.fm.2019.103243

    CAS  Article  PubMed  Google Scholar 

  9. dos Santos JLP, Samapundo S, Djunaidi S, Vermeulen A, Sant'Ana AS, Van Impe J, Devlieghere F (2020) Effect of storage temperature, water activity, oxygen headspace concentration and pasteurization intensity on the time to growth of Aspergillus fischerianus (teleomorph Neosartorya fischeri). Food Microbiol 88:103406. https://doi.org/10.1016/j.fm.2019.103406

    CAS  Article  PubMed  Google Scholar 

  10. Elkhishin MT, Gooneratne R, Hussain MA (2017) Microbial safety of foods in the supply chain and food security. Adv Food Technol Nutr Sci Open J 3:22–32. https://doi.org/10.17140/AFTNSOJ-3-141

    Article  Google Scholar 

  11. EU-European Union (2016) FUSIONS: Reducing food waste through social innovation. http://www.eu-fusions.org/phocadownload/Publications/Estimates%20of%20European%20food%20waste%20levels.pdf . Last accession November, 9th, 2020

  12. FAO-Food and Agriculture Organization of the United Nations (2012) Save Food: global initiative on food loss and waste reduction. http://www.fao.org/save-food/en/ . Last accession June, 22th, 2020.

  13. Greco M, Pardo A, Pose G, Patriarca A (2018) Effect of water activity and temperature on the growth of Eurotium species isolated from animal feeds. Rev Iberoam Micol 35:39–48. https://doi.org/10.1016/j.riam.2017.04.002

    Article  PubMed  Google Scholar 

  14. Grover DW, Nicol JM (1940) The vapour pressure of glycerin solution at 20 °C. J Chem Ind 59:175

    CAS  Google Scholar 

  15. Gysemans KPM, Bernaerts K, Vermeulen A, Geeraerd AH, Debevere J, Devlieghere F, Van Impe JF (2007) Exploring the performance of logistic regression model types on growth/no growth data of Listeria monocytogenes. Int J Food Microbiol 114:316–331. https://doi.org/10.1016/j.ijfoodmicro.2006.09.026

    CAS  Article  PubMed  Google Scholar 

  16. Hocking A, Pitt JI (1979) Water relations of some Penicillium species at 25 °C. Trans Br Mycol Soc 73:141–145. https://doi.org/10.4172/2157-7110.1000702

    CAS  Article  Google Scholar 

  17. King AD, Michener HD, Ito KA (1969) Control of Byssochlamys and related heat-resistant fungi in grape products. J Appl Microbiol 18:166–173

    CAS  Article  Google Scholar 

  18. King AD, Whitehand LC (1990) Alteration of Talaromyces flavus heat resistance by growth conditions and heating medium composition. J Food Sci 55:830–832. https://doi.org/10.1111/j.1365-2621.1990.tb05241.x

    Article  Google Scholar 

  19. Manusia SA, Berni E (2017) Inhibiting and inactivating effect of chitosan on heat resistant moulds responsible for spoilage of pasteurized fruit products. J Food Process Technol 8:1000702. https://doi.org/10.4172/2157-7110.1000702

    CAS  Article  Google Scholar 

  20. Nielsen PV (1991) Preservative and temperature effect on growth of three varieties of the heat-resistant mold, Neosartorya fischeri, as measured by an impedimetric method. J Food Sci 56:1735–1740. https://doi.org/10.1111/j.1365-2621.1991.tb08683.x

    CAS  Article  Google Scholar 

  21. Nielsen PV, Beuchat LR, Frisvad JC (1988) Growth of and fumitremorgin production by Neosartorya Fischeri as affected by temperature, light, and water activity. Appl Environ Microbiol 54:1504–1510

    CAS  Article  Google Scholar 

  22. Panagou EZ, Chelonas S, Chatzipavlidis I, Nychas GJE (2010) Modelling the effect of temperature and water activity on the growth rate and growth/no growth interface of Byssochlamys fulva and Byssochlamys nivea. Food Microbiol 27:618–627. https://doi.org/10.1016/j.fm.2010.02.005

    Article  PubMed  Google Scholar 

  23. Panagou EZ, Skandamis P, Nychas GJ (2003) Modelling the combined effect of temperature, pH and aw on the growth rate of Monascus ruber, a heat-resistant fungus isolated from green table olives. J Appl Microbiol 94:146–156. https://doi.org/10.1046/j.1365-2672.2003.01818.x

    CAS  Article  PubMed  Google Scholar 

  24. Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, New York

    Book  Google Scholar 

  25. Rico-Munoz E (2017) Heat resistant molds in foods and beverages: recent advances on assessment and prevention. Curr Opin Food Sci 17:75–83. https://doi.org/10.1016/j.cofs.2017.10.011

    Article  Google Scholar 

  26. Rico-Munoz E, dos Santos JLP (2019) The fungal problem in thermal processed beverages. Curr Opin Food Sci 29:80–87. https://doi.org/10.1016/j.cofs.2019.08.003

    Article  Google Scholar 

  27. Roland JO, Beuchat LR (1984) Influence of temperature and water activity on growth and patulin production by Byssochlamys nivea in apple juice. Appl Environ Microbiol 47:205–207. https://doi.org/10.1128/aem.47.1.205-207.1984

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS-KNAW, Utrecht

    Google Scholar 

  29. Sato J, Takano K (2000) Identification of filamentous fungi isolated from aseptic filling system for tea beverages and their microbiological characteristics. Food Sci Technol Res 6:48–53. https://doi.org/10.3136/fstr.6.48

    Article  Google Scholar 

  30. Sato J, Takei K (2000) Fungicidal effect of peracetic acid preparation on Arthrinium sacchari and Chaetomium funicola isolated from a tea beverage manufacturing plant. Biocontrol Sci 5:121–126. https://doi.org/10.4265/bio.5.121

    CAS  Article  Google Scholar 

  31. Scaramuzza N, Cigarini M, Mutti P, Berni E (2020a) Sanitization of packaging and machineries in the food industry: Effect of hydrogen peroxide on ascospores and conidia of filamentous fungi. Int J Food Microbiol 316:108421. https://doi.org/10.1016/j.ijfoodmicro.2019.108421

    CAS  Article  PubMed  Google Scholar 

  32. Scaramuzza N, Mutti P, Cigarini M, Berni E (2020b) Effect of peracetic acid on ascospore-forming molds and test microorganisms used for bio-validations of sanitizing processes in food plants. Int J Food Microbiol 332:108772. https://doi.org/10.1016/j.ijfoodmicro.2020.108772

    CAS  Article  PubMed  Google Scholar 

  33. Snyder AB, Worobo RW (2018) The incidence and impact of microbial spoilage in the production of fruit and vegetable juices as reported by juice manufacturers. Food Control 85:144–150. https://doi.org/10.1016/j.foodcont.2017.09.025

    Article  Google Scholar 

  34. Straus DC (2011) The possible role of fungal contamination in sick building syndrome. Front Biosci 3:562–580. https://doi.org/10.2741/e270

    Article  Google Scholar 

  35. Sturm K, Koron D, Stampar F (2003) The composition of fruit of different strawberry varieties, depending on maturity stage. Food Chem 83:417–422. https://doi.org/10.1016/S0308-8146(03)00124-9

    CAS  Article  Google Scholar 

  36. Taniwaki MH, Hocking AD, Pitt JI, Fleet GH (2001) Growth of fungi and mycotoxin production on cheese under modified atmospheres. Int J Food Microbiol 68:125–133. https://doi.org/10.1016/s0168-1605(01)00487-1

    CAS  Article  PubMed  Google Scholar 

  37. Tournas V, Traxler RW (1994) Heat resistance of a Neosartorya fischeri strain isolated from pineapple juice frozen concentrate. J Food Prot 57:814–816. https://doi.org/10.4315/0362-028X-57.9.814

    Article  PubMed  Google Scholar 

  38. Tranquillini R, Scaramuzza N, Berni E (2017) Occurrence and ecological distribution of heat resistant moulds spores (HRMS) in raw materials used by food industry and thermal characterization of two Talaromyces isolates. Int J Food Microbiol 242:116–123. https://doi.org/10.1016/j.ijfoodmicro.2016.11.023

    Article  PubMed  Google Scholar 

  39. Valík L, Piecková E (2001) Growth modelling of heat-resistant fungi: the effect of water activity. Int J Food Microbiol 63:11–17. https://doi.org/10.1016/S0168-1605(00)00386-X

    Article  PubMed  Google Scholar 

  40. Zimmermann M, Miorelli S, Massaguer PR, Aragao G (2011) Modeling the influence of water activity and ascospore age on the growth of Neosartorya fischeri in pineapple juice. LWT Food Sci Technol 44:239–243. https://doi.org/10.1016/j.lwt.2010.06.034

    CAS  Article  Google Scholar 

Download references

Acknowledgements

N/A

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Affiliations

Authors

Contributions

IR carried out all experiments. NS made contributions to acquisition, analysis, and interpretation of data. AH performed both the statistical analysis and the development of growth/no growth models, being actively involved in drafting and revision of the manuscript. EB has made substantial contribution to the study design of the experiments and wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Alyssa Hidalgo.

Ethics declarations

Ethics approval and consent to participate

This research does not contain any studies with human participants or animals.

Consent for publication

Informed consent is not applicable in this work.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Racchi, I., Scaramuzza, N., Hidalgo, A. et al. Combined effect of water activity and pH on the growth of food-related ascospore-forming molds. Ann Microbiol 70, 69 (2020). https://doi.org/10.1186/s13213-020-01612-6

Download citation

Keywords

  • Water activity
  • pH
  • Growth tests
  • Talaromyces
  • Neosartorya
  • Chaetomium