Spatial and compositional variation in the fungal communities of organic and conventionally grown apple fruit at the consumer point-of-purchase

Abstract

The fungal diversity in harvested apples from organic or conventional management practices was analyzed in different fruit locations (stem end, calyx end, peel, and wounded flesh) shortly after fruit purchase (T1) and after 2 weeks of storage (T5). A total of 5,760,162 high-quality fungal sequences were recovered and assigned to 8,504 Operational Taxonomic Units. Members of the phylum Ascomycota were dominant in all samples and accounted for 91.6% of the total number of detected sequences. This was followed by Basidiomycota (8%), Chytridiomycota (0.1%), and unidentified fungi (0.3%). Alpha and beta diversity analyses revealed the presence of significantly different fungal populations in the investigated fruit parts. Among detected fungi, the genus Penicillium prevailed in the peel and in the wounded flesh while Alternaria spp. prevailed in the calyx and stem end samples that included apple core tissues. Several taxonomic units that appear to be closely related to pathogenic fungi associated with secondary human infections were present in peel and wounds. Moreover, significantly different populations were revealed in organic and conventional apples and this result was consistent in all investigated fruit parts (calyx end, peel, stem end, and wounded flesh). Several unique taxa were exclusively detected in organic apples suggesting that management practices may have been a contributing factor in determining the taxa present. In contrast, little differences were revealed in the two assessment times (T1 and T5). Results of the present study represent an advancement of the current knowledge on the fungal microbiota in collected fruit tissues of apple.

Figure 1

Boxplots visualizing results of the nonparametric two-sample t-test based on Shannon diversity to compare the alpha diversity of fungal communities associated to different fruit parts (a), conventional and organic apples (b), and different assessment times (c). Analyzed fruit parts comprised calyx end (CE), peel (PE), stem end (SE), and wounded flesh (WF), and were collected from organic and conventional ‘Golden Delicious’ apples within a day after purchasing (T1), and after two weeks (T5) of storage at room temperature.

Figure 2

Sunburst chart showing the total relative abundance of fungal phyla (interior circle) and classes (exterior circle) overall detected in investigated samples.

Figure 3

Relative abundance (RA) of fungal genera (RA⩾1%) detected in peel (PE), wounded flesh (WF), calyx end (CE), and stem send (SE) of conventional and organic apples. Fungal genera with a cumulative RA<1% are reported as ‘other taxa’. Percentages reported in the legend along with fungal genera represents the average RA in the four investigated locations.

Figure 4

Network figures comparing fungal populations of conventional (Conv.) and organic (Org.) apples in the calyx end (a), stem end (b), wounded flesh (c), and peel (d). Networks were constructed regardless of time (using data from both T1 and T5 assessment times) and considering only significantly different taxa (P<0.01) with a cumulative RA in organic and conventional apples ⩾0.1%. Investigated samples were represented by large yellow nodes. Detected taxa were represented by green (Ascomycota), red (Basidiomycota), and blue (Unidentified fungi) nodes. The size of nodes is proportional to the cumulative RA of each taxon in all investigated samples. Similarly, the percentage values reported along taxa represent the cumulative RA of each taxon in all investigated samples. On the contrary, the width of line connecting samples and fungal taxa is proportional to the amount of each specific taxon in each specific sample.

Figure 5

Representative, fungal taxa detected with a significantly different relative abundance in organic and conventional apples.

Figure 6

Principal coordinate analysis (PCoA) of fungal populations associated to apples calyx end (CE), stem end (CE), Peel (PE), and Wounded flesh (WF) based on the beta diversity metric Bray Curtis. Analyses were performed considering sequences from both assessment times (T1 and T5) and from both conventional and organic apples.

Figure 7

Network figure comparing fungal populations detected in the calyx end (CE), stem end (CE), wounded flesh (WF), and peel (PE) of apple fruit. Networks were constructed using significantly different taxa (P<0.01) with a cumulative RA⩾0.1% and sequences from both assessment times (T1 and T5), and from both conventional and organic apples. Investigated samples were represented by large yellow nodes. Detected taxa were represented by green (Ascomycota), red (Basidiomycota), and blue (Unidentified fungi) nodes. The size of nodes is proportional to the cumulative RA of each taxon in all investigated samples. Similarly, the percentage values reported along taxa represent the cumulative RA of each taxon in all investigated samples. On the contrary, the width of line connecting samples and fungal taxa is proportional to the amount of each specific taxon in each specific sample location. Identified groups comprised taxa shared by all investigated locations (e), and taxa shared by CE and SE (a), WF and PE (b), CE, SE, and PE (c), and SE, PE, and WF (d), and unique to PE (f).

Figure 8

Network figures comparing fungal populations soon after fruit purchasing (T1) and after two weeks of storage (T5) in the calyx end (CE), stem end (SE), wounded flesh (WF), and peel (PE) of apple fruits. Networks were constructed regardless of practice (using data from organic and conventional apples) and considering only significantly different taxa (P<0.01) with a cumulative RA in organic and conventional apples ⩾0.1%. Investigated samples were represented by large yellow nodes. Detected taxa were represented by green (Ascomycota), red (Basidiomycota), and blue (Unidentified fungi) nodes. The size of nodes is proportional to the cumulative RA of each taxon in all investigated samples. Similarly, the percentage values reported along taxa represent the cumulative RA of each taxon in all investigated samples. On the contrary, the width of line connecting samples and fungal taxa is proportional to the amount of each specific taxon in each specific sample.