Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Systems Microbiology".

Deadline for manuscript submissions: closed (30 June 2020) | Viewed by 43865

Special Issue Editors


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Guest Editor
Dept. Postharvest Science, ARO, The Volcani Center, Rishon Lezion 7505101, Israel
Interests: biocontrol; fruit microbiome; host-pathogen interactions; fruit susceptibility and resistance; pathogenicity mechanisms

E-Mail Website
Guest Editor
Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Kearneysville, WV 25443, USA
Interests: microbiome evolution; apple microbiome; postharvest biocontrol; host-pathogen interactions

Special Issue Information

Dear Colleagues,

Microbiome studies are rapidly evolving, and new discoveries are changing the way we think about the biology of organisms, their interactions with the environment, and with the microbial world in general. New applications for the use of microbes and commercial opportunities are being created. A greater understanding of the fruit microbiome will lead to new strategies for preserving the quality and safety of harvested produce, an essential aspect of increasing food availability and sustainability.

The carposphere, represents a unique environment where nutrient levels may vary with age and a host of unique volatiles may be emitted. While the challenges posed by this new frontier are many, there are also great opportunities for the development of functionally-based biocontrol systems and biologically-based strategies for managing postharvest physiological disorders.

This Special Issue of Microorganisms will be dedicated to the following themes: the microbiome in plant health and disease; the microbiome in relation to postharvest biology and biological control; manipulating the fruit microbiome to suppress food-borne pathogens; challenges and tools of microbiome research (standardization, taxonomy, data analysis); practical application of microbiome research to postharvest pathology and biology; functional analysis of microbial communities on fruit surfaces; and plant microbiome in relation to food quality and safety.

Prof. Samir Droby
Dr. Michael Wisniewski
Guest Editors

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Keywords

  • biological control
  • postharvest diseases
  • fruit endopytes
  • fruit epiphytes
  • microbial networks
  • food quality

Published Papers (11 papers)

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15 pages, 1642 KiB  
Article
Dynamics of the Apple Fruit Microbiome after Harvest and Implications for Fruit Quality
by Yvonne Bösch, Elisabeth Britt, Sarah Perren, Andreas Naef, Jürg E. Frey and Andreas Bühlmann
Microorganisms 2021, 9(2), 272; https://doi.org/10.3390/microorganisms9020272 - 28 Jan 2021
Cited by 20 | Viewed by 3997
Abstract
The contribution of the apple microbiome to the production chain of apple was so far largely unknown. Here, we describe the apple fruit microbiome and influences on its composition by parameters such as storage season, storage duration, storage technology, apple variety, and plant [...] Read more.
The contribution of the apple microbiome to the production chain of apple was so far largely unknown. Here, we describe the apple fruit microbiome and influences on its composition by parameters such as storage season, storage duration, storage technology, apple variety, and plant protection schemes. A combined culturing and metabarcoding approach revealed significant differences in the abundance, composition, and diversity of the apple fruit microbiome. We showed that relatively few genera contribute a large portion of the microbiome on fruit and that the fruit microbiome changes during the storage season depending on the storage conditions. In addition, we show that the plant protection regime has an influence on the diversity of the fruit microbiome and on the dynamics of pathogenic fungal genera during the storage season. For the genus Neofabraea, the quantitative results from the metabarcoding approach were validated with real-time PCR. In conclusion, we identified key parameters determining the composition and temporal changes of the apple fruit microbiome, and the main abiotic driving factors of microbiome diversity on apple fruit were characterized. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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14 pages, 442 KiB  
Article
Optimization of a Method for the Concentration of Genetic Material in Bacterial and Fungal Communities on Fresh Apple Peel Surfaces
by Alexis Hamilton, Scott J. Harper and Faith Critzer
Microorganisms 2020, 8(10), 1480; https://doi.org/10.3390/microorganisms8101480 - 26 Sep 2020
Cited by 2 | Viewed by 2580
Abstract
Apples are the most consumed fruit in the United States and have recently been shown to exhibit some vulnerability to contamination across the supply chain. It is unclear what role a fruit microbiome analysis may serve in future food safety programs interested in [...] Read more.
Apples are the most consumed fruit in the United States and have recently been shown to exhibit some vulnerability to contamination across the supply chain. It is unclear what role a fruit microbiome analysis may serve in future food safety programs interested in understanding changes in the product and the processing environment. Ultimately, sample integrity is key if any of these approaches are to be employed; low microbial loads on apple surfaces, the inability to sample the entire surface, and inefficiency of removal may act as barriers to achieving high-quality DNA. As such, the objective of this study was to identify a reproducible method to concentrate and quantify bacterial and fungal DNA from fresh apple surfaces. Five methods were evaluated: two variations of wash solutions for bath sonication, wash filtration, epidermis excision, and surface swabbing. Epidermis excision returned the highest mean DNA quantities, followed by the sonicated washes and wash filtration. Surface swabbing was consistently below the limit of detection. Based on the quantity of host DNA contamination in surface excision, the sonicated wash solution containing a surfactant presents the greatest opportunity for consistent, high-yielding DNA recovery from the entire apple surface. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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21 pages, 7030 KiB  
Article
Effect of Washing, Waxing and Low-Temperature Storage on the Postharvest Microbiome of Apple
by Ahmed Abdelfattah, Susan R. Whitehead, Dumitru Macarisin, Jia Liu, Erik Burchard, Shiri Freilich, Christopher Dardick, Samir Droby and Michael Wisniewski
Microorganisms 2020, 8(6), 944; https://doi.org/10.3390/microorganisms8060944 - 23 Jun 2020
Cited by 52 | Viewed by 5644
Abstract
There is growing recognition of the role that the microbiome plays in the health and physiology of many plant species. However, considerably less research has been conducted on the postharvest microbiome of produce and the impact that postharvest processing may have on its [...] Read more.
There is growing recognition of the role that the microbiome plays in the health and physiology of many plant species. However, considerably less research has been conducted on the postharvest microbiome of produce and the impact that postharvest processing may have on its composition. Here, amplicon sequencing was used to study the effect of washing, waxing, and low-temperature storage at 2 °C for six months on the bacterial and fungal communities of apple calyx-end, stem-end, and peel tissues. The results of the present work reveal that tissue-type is the main factor defining fungal and bacterial diversity and community composition on apple fruit. Both postharvest treatments and low temperature storage had a strong impact on the fungal and bacterial diversity and community composition of these tissue types. Distinct spatial and temporal changes in the composition and diversity of the microbiota were observed in response to various postharvest management practices. The greatest impact was attributed to sanitation practices with major differences among unwashed, washed and washed-waxed apples. The magnitude of the differences, however, was tissue-specific, with the greatest impact occurring on peel tissues. Temporally, the largest shift occurred during the first two months of low-temperature storage, although fungi were more affected by storage time than bacteria. In general, fungi and bacteria were impacted equally by sanitation practices, especially the epiphytic microflora of peel tissues. This research provides a foundation for understanding the impact of postharvest management practices on the microbiome of apple and its potential subsequent effects on postharvest disease management and food safety. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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11 pages, 1643 KiB  
Article
NetMet: A Network-Based Tool for Predicting Metabolic Capacities of Microbial Species and their Interactions
by Ofir Tal, Gopinath Selvaraj, Shlomit Medina, Shany Ofaim and Shiri Freilich
Microorganisms 2020, 8(6), 840; https://doi.org/10.3390/microorganisms8060840 - 03 Jun 2020
Cited by 12 | Viewed by 3032
Abstract
Metabolic conversions allow organisms to produce a set of essential metabolites from the available nutrients in an environment, frequently requiring metabolic exchanges among co-inhabiting organisms. Genomic-based metabolic simulations are being increasingly applied for exploring metabolic capacities, considering different environments and different combinations of [...] Read more.
Metabolic conversions allow organisms to produce a set of essential metabolites from the available nutrients in an environment, frequently requiring metabolic exchanges among co-inhabiting organisms. Genomic-based metabolic simulations are being increasingly applied for exploring metabolic capacities, considering different environments and different combinations of microorganisms. NetMet is a web-based tool and a software package for predicting the metabolic performances of microorganisms and their corresponding combinations in user-defined environments. The algorithm takes, as input, lists of (i) species-specific enzymatic reactions (EC numbers), and (ii) relevant metabolic environments. The algorithm generates, as output, lists of (i) compounds that individual species can produce in each given environment, and (ii) compounds that are predicted to be produced through complementary interactions. The tool is demonstrated in two case studies. First, we compared the metabolic capacities of different haplotypes of the obligatory fruit and vegetable pathogen Candidatus Liberibacter solanacearum to those of their culturable taxonomic relative Liberibacter crescens. Second, we demonstrated the potential production of complementary metabolites by pairwise combinations of co-occurring endosymbionts of the plant phloem-feeding whitefly Bemisia tabaci. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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17 pages, 1136 KiB  
Article
Endophytes Increased Fruit Quality with Higher Soluble Sugar Production in Honeycrisp Apple (Malus pumila)
by Hyungmin Rho, Victor Van Epps, Soo-Hyung Kim and Sharon L. Doty
Microorganisms 2020, 8(5), 699; https://doi.org/10.3390/microorganisms8050699 - 10 May 2020
Cited by 17 | Viewed by 3532
Abstract
Endophytes are fungi, bacteria, or yeast symbionts that live in the intercellular spaces or vascular tissues of host plants. Investigations indicate that endophytes isolated from the Salicaceae family (Populus and Salix) hosts provide several benefits that promote plant growth, including but [...] Read more.
Endophytes are fungi, bacteria, or yeast symbionts that live in the intercellular spaces or vascular tissues of host plants. Investigations indicate that endophytes isolated from the Salicaceae family (Populus and Salix) hosts provide several benefits that promote plant growth, including but not limited to di-nitrogen fixation, plant hormone production, nutrient acquisition, stress tolerance, and defense against phytopathogens. In exchange, the microorganisms receive domicile and photosynthates. Considering the known characteristics of nitrogen fixation and plant hormone production, we hypothesized that apple trees grown under nitrogen-limited conditions would show improved biometrics with endophyte inoculation. Our research objectives were to investigate the endophyte effects on plant physiology and fruiting. We examined these effects through ecophysiology metrics involving rates of photosynthesis, stomatal conductance and density, transpiration, biomass accretion, chlorophyll content and fluorescence, and fruit soluble sugar content and biomass. Our results showed evidence of the endophytes’ colonization in apple trees, decreased stomatal density, delayed leaf senescence, and increased lateral root biomass with endophytes. A highlight of the findings was a significant increase in both fruit soluble sugar content and biomass. Future research into the mechanistic underpinnings of this phenomenon stands to offer novel insights on how microbiota may alter carbohydrate metabolism under nitrogen-deficient conditions. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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15 pages, 2080 KiB  
Article
Characterizing the Fungal Microbiome in Date (Phoenix dactylifera) Fruit Pulp and Peel from Early Development to Harvest
by Edoardo Piombo, Ahmed Abdelfattah, Yaara Danino, Shoshana Salim, Oleg Feygenberg, Davide Spadaro, Michael Wisniewski and Samir Droby
Microorganisms 2020, 8(5), 641; https://doi.org/10.3390/microorganisms8050641 - 28 Apr 2020
Cited by 19 | Viewed by 3900
Abstract
Date palm (Phoenix dactylifera) is considered to be a highly important food crop in several African and Middle Eastern countries due to its nutritional value and health-promoting properties. Microbial contamination of dates has been of concern to consumers, but very few [...] Read more.
Date palm (Phoenix dactylifera) is considered to be a highly important food crop in several African and Middle Eastern countries due to its nutritional value and health-promoting properties. Microbial contamination of dates has been of concern to consumers, but very few works have analyzed in detail the microbial load of the different parts of date fruit. In the present work, we characterized the fungal communities of date fruit using a metagenomic approach, analyzing the data for differences between microbial populations residing in the pulp and peel of “Medjool” dates at the different stages of fruit development. The results revealed that Penicillium, Cladosporium, Aspergillus, and Alternaria were the most abundant genera in both parts of the fruit, however, the distribution of taxa among the time points and tissue types (peel vs. pulp) was very diverse. Penicillium was more abundant in the pulp at the green developmental stage (Kimri), while Aspergillus was more frequent in the peel at the brown developmental stage (Tamer). The highest abundance of Alternaria was detected at the earliest sampled stage of fruit development (Hababauk stage). Cladosporium had a high level of abundance in peel tissues at the Hababauk and yellow (Khalal) stages. Regarding the yeast community, the abundance of Candida remained stable up until the Khalal stage, but exhibited a dramatic increase in abundance at the Tamer stage in peel tissues, while the level of Metschnikowia, a genus containing several species with postharvest biocontrol activity, exhibited no significant differences between the two tissue types or stages of fruit development. This work constitutes a comprehensive metagenomic analysis of the fungal microbiome of date fruits, and has identified changes in the composition of the fungal microbiome in peel and pulp tissues at the different stages of fruit development. Notably, this study has also characterized the endophytic fungal microbiome present in pulp tissues of dates. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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18 pages, 2641 KiB  
Article
Harvesting Mango Fruit with a Short Stem-End Altered Endophytic Microbiome and Reduce Stem-End Rot
by Ortal Galsurker, Sonia Diskin, Danielle Duanis-Assaf, Adi Doron-Faigenboim, Dalia Maurer, Oleg Feygenberg and Noam Alkan
Microorganisms 2020, 8(4), 558; https://doi.org/10.3390/microorganisms8040558 - 13 Apr 2020
Cited by 24 | Viewed by 4473
Abstract
Stem-end rot (SER) is a serious postharvest disease of mango fruit grown in semi-dry area. Pathogenic and non-pathogenic microorganisms endophytically colonize fruit stem-end. As fruit ripens, some pathogenic fungi switch from endophytic colonization to necrotrophic stage and cause SER. Various pre/post-treatments may alter [...] Read more.
Stem-end rot (SER) is a serious postharvest disease of mango fruit grown in semi-dry area. Pathogenic and non-pathogenic microorganisms endophytically colonize fruit stem-end. As fruit ripens, some pathogenic fungi switch from endophytic colonization to necrotrophic stage and cause SER. Various pre/post-treatments may alter the stem-end community and modify SER incidence. This study investigates the effects of harvesting mango with or without short stem-end on fruit antifungal and antioxidant activities, the endophytic microbiome, and SER during fruit storage. Our results show that harvesting mango with short stem significantly reduced SER during storage. At harvest, fruit harvested with or without stem exhibit a similar microorganisms community profile. However, after storage and shelf life, the community of fruit without stem shifted toward more SER-causing-pathogens, such as Lasiodiplodia, Dothiorella, and Alternaria, and separated from the community of fruit with stem. This change correlated to the high antifungal activity of stem extract that strongly inhibited both germination and growth of Lasiodiplodia theobromae and Alternaria alternata. Additionally, fruit that was harvested with stem displayed more antioxidant activity and less ROS. Altogether, these findings indicate that harvesting mango with short stem leads to higher antifungal and antioxidant activity, retaining a healthier microbial community and leading to reduced postharvest SER. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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18 pages, 3343 KiB  
Article
Fungal Microbiota of Sea Buckthorn Berries at Two Ripening Stages and Volatile Profiling of Potential Biocontrol Yeasts
by Juliana Lukša, Iglė Vepštaitė-Monstavičė, Violeta Apšegaitė, Laima Blažytė-Čereškienė, Ramunė Stanevičienė, Živilė Strazdaitė-Žielienė, Bazilė Ravoitytė, Dominykas Aleknavičius, Vincas Būda, Raimondas Mozūraitis and Elena Servienė
Microorganisms 2020, 8(3), 456; https://doi.org/10.3390/microorganisms8030456 - 23 Mar 2020
Cited by 11 | Viewed by 3761 | Correction
Abstract
Sea buckthorn, Hippophae rhamnoides L., has considerable potential for landscape reclamation, food, medicinal, and cosmetics industries. In this study, we analyzed fungal microorganism populations associated with carposphere of sea buckthorn harvested in Lithuania. An amplicon metagenomic approach based on the ITS2 region [...] Read more.
Sea buckthorn, Hippophae rhamnoides L., has considerable potential for landscape reclamation, food, medicinal, and cosmetics industries. In this study, we analyzed fungal microorganism populations associated with carposphere of sea buckthorn harvested in Lithuania. An amplicon metagenomic approach based on the ITS2 region of fungal rDNA was used to reveal the ripening-affected fungal community alterations on sea buckthorn berries. According to alpha and beta diversity analyses, depending on the ripening stage, sea buckthorn displayed significantly different fungal communities. Unripe berries were shown to be prevalent by Aureobasidium, Taphrina, and Cladosporium, while ripe berries were dominated by Aureobasidium and Metschnikowia. The selected yeast strains from unripe and mature berries were applied for volatile organic compounds identification by gas chromatography and mass spectrometry techniques. It was demonstrated that the patterns of volatiles of four yeast species tested were distinct from each other. The current study for the first time revealed the alterations of fungal microorganism communities colonizing the surface of sea buckthorn berries at different ripening stages. The novel information on specific volatile profiles of cultivable sea buckthorn-associated yeasts with a potential role in biocontrol is important for the development of the strategies for plant cultivation and disease management, as well as for the improvement of the quality and preservation of the postharvest berries. Management of the fungal microorganisms present on the surface of berries might be a powerful instrument for control of phytopathogenic and potentially antagonistic microorganisms affecting development and quality of the berries. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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16 pages, 4444 KiB  
Article
Yeasts and Bacterial Consortia from Kefir Grains Are Effective Biocontrol Agents of Postharvest Diseases of Fruits
by V. Yeka Zhimo, Antonio Biasi, Ajay Kumar, Oleg Feygenberg, Shoshana Salim, Silvana Vero, Michael Wisniewski and Samir Droby
Microorganisms 2020, 8(3), 428; https://doi.org/10.3390/microorganisms8030428 - 18 Mar 2020
Cited by 21 | Viewed by 5774
Abstract
Fungal pathogens in fruits and vegetables cause significant losses during handling, transportation, and storage. Biological control with microbial antagonists replacing the use of chemical fungicides is a major approach in postharvest disease control, and several products based on single antagonists have been developed [...] Read more.
Fungal pathogens in fruits and vegetables cause significant losses during handling, transportation, and storage. Biological control with microbial antagonists replacing the use of chemical fungicides is a major approach in postharvest disease control, and several products based on single antagonists have been developed but have limitations related to reduced and inconsistent performance under commercial conditions. One possible approach to enhance the biocontrol efficacy is to broaden the spectrum of the antagonistic action by employing compatible microbial consortia. Here, we explore commercial kefir grains, a natural probiotic microbial consortium, by culture-dependent and metagenomic approaches and observed a rich diversity of co-existing yeasts and bacterial population. We report effective inhibition of the postharvest pathogen Penicillium expansum on apple by using the grains in its fresh commercial and milk-activated forms. We observed few candidate bacteria and yeasts from the kefir grains that grew together over successive enrichment cycles, and these mixed fermentation cultures showed enhanced biocontrol activities as compared to the fresh commercial or milk-activated grains. We also report several individual species of bacteria and yeasts with biocontrol activities against Penicillium rots on apple and grapefruit. These species with antagonistic properties could be further exploited to develop a synthetic consortium to achieve enhanced antagonistic effects against a wide range of postharvest pathogens. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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17 pages, 1837 KiB  
Article
Standardization of Plant Microbiome Studies: Which Proportion of the Microbiota is Really Harvested?
by Abdoul Razack Sare, Gilles Stouvenakers, Mathilde Eck, Amber Lampens, Sofie Goormachtig, M. Haïssam Jijakli and Sebastien Massart
Microorganisms 2020, 8(3), 342; https://doi.org/10.3390/microorganisms8030342 - 28 Feb 2020
Cited by 15 | Viewed by 4717
Abstract
Studies in plant-microbiome currently use diverse protocols, making their comparison difficult and biased. Research in human microbiome have faced similar challenges, but the scientific community proposed various recommendations which could also be applied to phytobiome studies. Here, we addressed the isolation of plant [...] Read more.
Studies in plant-microbiome currently use diverse protocols, making their comparison difficult and biased. Research in human microbiome have faced similar challenges, but the scientific community proposed various recommendations which could also be applied to phytobiome studies. Here, we addressed the isolation of plant microbiota through apple carposphere and lettuce root microbiome. We demonstrated that the fraction of the culturable epiphytic microbiota harvested by a single wash might only represent one-third of the residing microbiota harvested after four successive washes. In addition, we observed important variability between the efficiency of washing protocols (up to 1.6-fold difference for apple and 1.9 for lettuce). QIIME2 analysis of 16S rRNA gene, showed a significant difference of the alpha and beta diversity between protocols in both cases. The abundance of 76 taxa was significantly different between protocols used for apple. In both cases, differences between protocols disappeared when sequences of the four washes were pooled. Hence, pooling the four successive washes increased the alpha diversity for apple in comparison to a single wash. These results underline the interest of repeated washing to leverage abundance of microbial cells harvested from plant epiphytic microbiota whatever the washing protocols, thus minimizing bias. Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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1 pages, 163 KiB  
Correction
Correction: Lukša, J., et al. Fungal Microbiota of Sea Buckthorn Berries at Two Ripening Stages and Volatile Profiling of Potential Biocontrol Yeasts. Microorganisms 2020, 8, 456
by Juliana Lukša, Iglė Vepštaitė-Monstavičė, Violeta Apšegaitė, Laima Blažytė-Čereškienė, Ramunė Stanevičienė, Živilė Strazdaitė-Žielienė, Bazilė Ravoitytė, Dominykas Aleknavičius, Vincas Būda, Raimondas Mozūraitis and Elena Servienė
Microorganisms 2020, 8(7), 1090; https://doi.org/10.3390/microorganisms8071090 - 21 Jul 2020
Cited by 3 | Viewed by 1628
Abstract
The authors wish to make the following corrections to this paper [...] Full article
(This article belongs to the Special Issue Applying Metaorganism Studies to the Fruit Microbiome: A New Frontier)
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