From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale

ABSTRACT Apples are affected by numerous fungi known as storage rots, which cause significant losses before and after harvest. Concerns about increasing antimicrobial resistance, bans on various fungicides, and changing consumer preferences are motivating the search for safer means to prevent fruit...

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Main Authors: Janja Zajc, Anja Černoša, Xiaohuan Sun, Chao Fang, Nina Gunde-Cimerman, Zewei Song, Cene Gostinčar
Format: Article
Language:English
Published: American Society for Microbiology 2022-08-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.01455-22
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author Janja Zajc
Anja Černoša
Xiaohuan Sun
Chao Fang
Nina Gunde-Cimerman
Zewei Song
Cene Gostinčar
author_facet Janja Zajc
Anja Černoša
Xiaohuan Sun
Chao Fang
Nina Gunde-Cimerman
Zewei Song
Cene Gostinčar
author_sort Janja Zajc
collection DOAJ
description ABSTRACT Apples are affected by numerous fungi known as storage rots, which cause significant losses before and after harvest. Concerns about increasing antimicrobial resistance, bans on various fungicides, and changing consumer preferences are motivating the search for safer means to prevent fruit rot. The use of antagonistic microbes has been shown to be an efficient and environmentally friendly alternative to conventional phytopharmaceuticals. Here, we investigate the potential of Aureobasidium subglaciale for postharvest rot control. We tested the antagonistic activity of 9 strains of A. subglaciale and 7 closely related strains against relevant phytopathogenic fungi under conditions simulating low-temperature storage: Botrytis cinerea, Penicillium expansum, and Colletotrichum acutatum. We also investigated a selection of phenotypic traits of all strains and sequenced their whole genomes. The tested strains significantly reduced postharvest rot of apples at low temperatures caused by B. cinerea, C. acutatum (over 60%), and P. expansum (about 40%). Several phenotypic traits were observed that may contribute to this biocontrol capacity: growth at low temperatures, tolerance to high temperatures and elevated solute concentrations, and strong production of several extracellular enzymes and siderophores. Population genomics revealed that 7 of the 15 strains originally identified as A. subglaciale most likely belong to other, possibly undescribed species of the same genus. In addition, the population structure and linkage disequilibrium of the species suggest that A. subglaciale is strictly clonal and therefore particularly well suited for use in biocontrol. Overall, these data suggest substantial biological control potential for A. subglaciale, which represents another promising biological agent for disease control in fresh fruit. IMPORTANCE After harvest, fruits are often stored at low temperatures to prolong their life. However, despite the low temperatures, much of the fruit is lost to rot caused by a variety of fungi, resulting in major economic losses and food safety risks. An increasingly important environmentally friendly alternative to conventional methods of mitigating the effects of plant diseases is the use of microorganisms that act similarly to probiotics—occupying the available space, producing antimicrobial compounds, and consuming the nutrients needed by the rot-causing species. To find a new microorganism for biological control that is particularly suitable for cold storage of fruit, we tested different isolates of the cold-loving yeast Aureobasidium subglaciale and studied their phenotypic characteristics and genomes. We demonstrated that A. subglaciale can significantly reduce rotting of apples caused by three rot-causing molds at low temperatures and thus has great potential for preventing fruit rot during cold storage.
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spelling doaj.art-5754ff39d03547739760c2d04820d2f22022-12-22T03:44:53ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.01455-22From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglacialeJanja Zajc0Anja Černoša1Xiaohuan Sun2Chao Fang3Nina Gunde-Cimerman4Zewei Song5Cene Gostinčar6Plant Protection Department, Agricultural Institute of Slovenia, Ljubljana, SloveniaDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaBGI-Shenzhen, Shenzhen, ChinaBGI-Shenzhen, Shenzhen, ChinaDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaBGI-Shenzhen, Shenzhen, ChinaDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaABSTRACT Apples are affected by numerous fungi known as storage rots, which cause significant losses before and after harvest. Concerns about increasing antimicrobial resistance, bans on various fungicides, and changing consumer preferences are motivating the search for safer means to prevent fruit rot. The use of antagonistic microbes has been shown to be an efficient and environmentally friendly alternative to conventional phytopharmaceuticals. Here, we investigate the potential of Aureobasidium subglaciale for postharvest rot control. We tested the antagonistic activity of 9 strains of A. subglaciale and 7 closely related strains against relevant phytopathogenic fungi under conditions simulating low-temperature storage: Botrytis cinerea, Penicillium expansum, and Colletotrichum acutatum. We also investigated a selection of phenotypic traits of all strains and sequenced their whole genomes. The tested strains significantly reduced postharvest rot of apples at low temperatures caused by B. cinerea, C. acutatum (over 60%), and P. expansum (about 40%). Several phenotypic traits were observed that may contribute to this biocontrol capacity: growth at low temperatures, tolerance to high temperatures and elevated solute concentrations, and strong production of several extracellular enzymes and siderophores. Population genomics revealed that 7 of the 15 strains originally identified as A. subglaciale most likely belong to other, possibly undescribed species of the same genus. In addition, the population structure and linkage disequilibrium of the species suggest that A. subglaciale is strictly clonal and therefore particularly well suited for use in biocontrol. Overall, these data suggest substantial biological control potential for A. subglaciale, which represents another promising biological agent for disease control in fresh fruit. IMPORTANCE After harvest, fruits are often stored at low temperatures to prolong their life. However, despite the low temperatures, much of the fruit is lost to rot caused by a variety of fungi, resulting in major economic losses and food safety risks. An increasingly important environmentally friendly alternative to conventional methods of mitigating the effects of plant diseases is the use of microorganisms that act similarly to probiotics—occupying the available space, producing antimicrobial compounds, and consuming the nutrients needed by the rot-causing species. To find a new microorganism for biological control that is particularly suitable for cold storage of fruit, we tested different isolates of the cold-loving yeast Aureobasidium subglaciale and studied their phenotypic characteristics and genomes. We demonstrated that A. subglaciale can significantly reduce rotting of apples caused by three rot-causing molds at low temperatures and thus has great potential for preventing fruit rot during cold storage.https://journals.asm.org/doi/10.1128/spectrum.01455-22cold adaptedgenome analysisantagonismstorage rotapple decay
spellingShingle Janja Zajc
Anja Černoša
Xiaohuan Sun
Chao Fang
Nina Gunde-Cimerman
Zewei Song
Cene Gostinčar
From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale
Microbiology Spectrum
cold adapted
genome analysis
antagonism
storage rot
apple decay
title From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale
title_full From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale
title_fullStr From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale
title_full_unstemmed From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale
title_short From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale
title_sort from glaciers to refrigerators the population genomics and biocontrol potential of the black yeast aureobasidium subglaciale
topic cold adapted
genome analysis
antagonism
storage rot
apple decay
url https://journals.asm.org/doi/10.1128/spectrum.01455-22
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