Alternaria in Food: Ecophysiology, Mycotoxin Production and Toxicology

Abstract

Alternaria species are common saprophytes or pathogens of a wide range of plants pre- and post-harvest. This review considers the relative importance of Alternaria species, their ecology, competitiveness, production of mycotoxins and the prevalence of the predominant mycotoxins in different food products. The available toxicity data on these toxins and the potential future impacts of Alternaria species and their toxicity in food products pre- and post-harvest are discussed. The growth of Alternaria species is influenced by interacting abiotic factors, especially water activity (aw), temperature and pH. The boundary conditions which allow growth and toxin production have been identified in relation to different matrices including cereal grain, sorghum, cottonseed, tomato, and soya beans. The competitiveness of Alternaria species is related to their water stress tolerance, hydrolytic enzyme production and ability to produce mycotoxins. The relationship between A. tenuissima and other phyllosphere fungi has been examined and the relative competitiveness determined using both an Index of Dominance (ID) and the Niche Overlap Index (NOI) based on carbon-utilisation patterns. The toxicology of some of the Alternaria mycotoxins have been studied; however, some data are still lacking. The isolation of Alternaria toxins in different food products including processed products is reviewed. The future implications of Alternaria colonization/infection and the role of their mycotoxins in food production chains pre- and post-harvest are discussed.

Keywords: Alternaria species; Ecology; Food products; Mycotoxins; Physiology.

Fig. 1. Neighbor-joining phylogenetic tree showing 24 sections including Alternata, Alternantherae, and Sonchi in Alternaria complex belonging to Ploeosporaceae based on internal transcribed spacer rDNA sequences. Bootstrap percentages are presented at the nodes. The monotypic lineages are indicated by black dots based on the phylogeny constructed by Woudenberg et al. [12].

Fig. 2. Structure of the different toxins produced by Alternaria species. Key to toxins: AOH, alternariol; AME, alternariol monomethyl ether; iso-ALT, iso-altenuene; TeA, tenuazonic acid; iso-TeA, iso-tenuazonic acid; TEN, tentoxin; ATX-I, altertoxin I; ATX-II, altertoxin II; ATX-III, altertoxin III; STTX III, Stemphyltoxin III; AAL TA1 and TA2 toxin, Alternaria alternata f. sp. lycopersici TA1 and TA2 toxin; fumonisin B1.

Fig. 3. A, Effect of water activity (a_w) × temperature effects on growth of a strain of Alternaria alternata on a wheat-based medium; B, The growth profile of A. alternata on wheat-based medium showing the optimum and boundary conditions for growth. Numbers on the isopleths join conditions with a similar growth rate (mm/day). Adopted from Magan N and Aldred D [18].

Fig. 4. The effect of water activity (a_w) and time on the specific activity of 5 different hydrolytic enzymes by a strain of Alternaria tenuissima on wheat grain. Please note the difference in scale for one of the enzymes. Adopted from Hope R [26].

Fig. 5. Diagramatic example of the impact of environmental factors on Niche sizes (dotted line circle: Alternaria alternata [NS alt]; solid line circle: A. ochraceus [NS och]) and Niche Overlap Index (NOI) between A. alternata and Aspergillus ochraceus. Modified from Magan N and Aldred D [18] and Lee HB and Magan N [29].

Fig. 6. Comparison of water activity (a_w) × temperature conditions over which growth and three different Alternaria mycotoxins can be produced on wheat. Adopted from Sanchis V and Magan N [34].

Fig. 7. Kinetics of altertoxin-II (ATX-II) production by two strains of Alternaria tennuissima over periods of 14 and 21 days on wheat-based medium. Bars indicate standard errors. Please note different Y-axis range for 0.98 and 0.95 water activities. Adopted from Patriarca A et al. [19].