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Metschnikowia Pulcherrima and Related Pulcherrimin-Producing Yeasts: Fuzzy Species Boundaries and Complex Antimicrobial Antagonism

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Metschnikowia Pulcherrima and Related Pulcherrimin-Producing Yeasts: Fuzzy Species Boundaries and Complex Antimicrobial Antagonism microorganisms Review Metschnikowia pulcherrima and Related Pulcherrimin-Producing Yeasts: Fuzzy Species Boundaries and Complex Antimicrobial Antagonism Matthias Sipiczki Department of Genetics and Applied Microbiology, University of Debrecen, 4032 Debrecen, Hungary; [email protected] Received: 29 June 2020; Accepted: 10 July 2020; Published: 12 July 2020 Abstract: Yeasts affiliated with the Metschnikowia pulcherrima clade (subclade) of the large ascomycetous genus Metschnikowia frequently turn out to produce the characteristic maroon-red pulcherrimin when tested for pigment production and prove to exert antagonistic effects on many types of microorganisms. The determination of the exact taxonomic position of the strains is hampered by the shortage of distinctive morphological and physiological properties of the species of the clade and the lack of rDNA barcode gaps. The rDNA repeats of the type strains of the species are not homogenized and are assumed to evolve by a birth-and-death mechanism combined with reticulation. The taxonomic division is further hampered by the incomplete biological (reproductive) isolation of the species: certain type strains can be hybridized and genome sequencing revealed chimeric genome structures in certain strains that might have evolved from interspecies hybrids (alloploid genome duplication). Various mechanisms have been proposed for the antimicrobial antagonism. One is related to pulcherrimin production. The diffusible precursor of pulcherrimin, the pulcherriminic acid is secreted by the cells into the environment where it forms the insoluble pulcherrimin with the ferric ions. The lack of free iron caused by the immobilization of ferric ions inhibits the growth of many microorganisms. Recent results of research into the complexity of the taxonomic division of the pulcherrimin-producing Metschnikowia yeasts and the mechanism(s) underlying their antimicrobial antagonism are discussed in this review. Keywords: Metschnikowia; taxonomy; barcodes; genome; reticulation; antagonism; pulcherrimin; iron-depletion; bioprotection 1. Introduction Metschnikowia Kamienski (1899) is a large ascomycetous genus currently comprising 79 species (Mycobank, 04. 2020) but the number or species is continuously growing. The M. pulcherrima clade of the genus contains seven validly described species that share the ability to produce pulcherrimin, a maroon-red pigment (reviewed in [1,2]). These species and the strains closely related to them have broad biotechnological potential for application in various industrial processes. In wine fermentation, these yeasts can modulate the population dynamics of the fermenting yeast communities and produce enzymes and a broad range of compounds that improve the aromatic complexity of the wine (for a review, see [3]). Due to the large fatty globules in their chlamydospores (“pulcherrima cells”), the strains are outstanding candidates for low-cost lipid production (reviewed in [4]). Their most intensively studied property is the strong antimicrobial activity (Figure1A–C) (e.g., [ 5–12]). Since the mechanisms underlying their antagonistic effect are not associated with the production of toxic compounds, these strains can safely be used as bioprotective agents to curb the invasion of pathogenic and rotting (saprophytic) microorganisms (Figure1D) and /or additives in food technologies Microorganisms 2020, 8, 1029; doi:10.3390/microorganisms8071029 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, x FOR PEER REVIEW 2 of 19 Microorganisms 2020, 8, 1029 2 of 19 invasion of pathogenic and rotting (saprophytic) microorganisms (Figure 1D) and/or additives in food technologies to modulate the dynamics of microbial populations. Numerous technological innovationsto modulate involving the dynamics antagonistic of microbial Metschnikowia populations. strains Numerous have been technological patented innovations (e.g., JPH01117778A, involving 1989;antagonistic US6991930B1,Metschnikowia 2006; NZ528225A,strains have 2008; been P0800 patented775, (e.g.,2008; JPH01117778A,ITTO20070655A1, 1989; 2009; US6991930B1, WO2010149370, 2006; 2010;NZ528225A, WO2010149369, 2008; P0800775, 2010; 2008; CN101946805A ITTO20070655A1, 2011 2009;; CN103642705A, WO2010149370, 2014; 2010; EP3266305A1, WO2010149369, 2018; 2010; CN107904180A,CN101946805A 2011;2018; CN103642705A, CN110684678A, 2014; 2020;) EP3266305A1, and several 2018; Metschnikowia- CN107904180A,based 2018;products CN110684678A, have been commercialiZed2020;) and several [ExcellenceMetschnikowia- Bio-Naturebased products (Lamothe-Abiet), have been commercialiZedFlavia and Gaïa [Excellence (Lallemand), Bio-Nature Shemer (Bayer,(Lamothe-Abiet), Koppert Biological Flavia and GaïaSystems) (Lallemand), Zymaflore Shemer Egide (Bayer, (Laffort)] Koppert as ADYs Biological (Active Systems) Dry ZymafloreYeast) for inoculatedEgide (Laff ort)]fermentation as ADYs (Activeor as biocontrol Dry Yeast) agents for inoculated for application fermentation against or asplant biocontrol pathogens agents and for post-harvestapplication against plant diseases. plant pathogens and post-harvest plant diseases. Figure 1. PigmentPigment production production and and antagonism. antagonism. ( (AA)) Pigmented Pigmented halos halos around around the the colonies colonies of of the Metschnikowia strainstrain 02.11.1.21. 02.11.1.21. ( B(B) Inhibition) Inhibition zone zone around around the the colony colony of the of same the same strain strain (1: Botrytis (1: Botrytis cinerea cinerea3318, 2: 3318,Saccharomyces 2: Saccharomyces cerevisiae S288c,cerevisiae 3: Metschnikowia S288c, 3: Metschnikowia02.11.1.21). ( C02.11.1.21).) Coincidence (C of) Coincidence pigmented halo of pigmentedand inhibition halo zone and around inhibition the colonyzone around of Metschnikowia the colony02.11.1.21 of Metschnikowia on a medium 02.11.1.21 supplemented on a medium with supplemented0.005 mg/mL FeCl with3 and0.005mg/ml flooded FeCl with3 conidiaand flooded of B. with cinerea conidia3318. (ofD )B. Inhibition cinerea 3318. of rotting(D) Inhibition caused byof rottingBotrytis caused(1: untreated, by Botrytis 2: dipped (1: untreated, in a suspension 2: dippedMetschnikowia in a suspension02.11.1.21 Metschnikowia cells, 3: dipped02.11.1.21 in acells, mixed 3: dippedsuspension in a ofmixedB. cinerea suspension3318 conidia of B. cinerea and Metschnikowia 3318 conidia 02.11.1.21and Metschnikowia cells, 4: dipped02.11.1.21 in acells, suspension 4: dipped of inB. a cinerea suspension3318 conidia). of B. cinerea See reference3318 conidia). [6] for See the reference description [6] for of thethe strains.description of the strains. Over the past two decades, large numbers of strain strainss isolated from various substrates have been assigned to one or the other of these species (preferentially to M. pulcherrima ) on on the the basis basis of of barcode barcode sequence (preferentially(preferentially the the D1 D1/D2/D2 domains domains of the of LSUthe rRNALSU rRNA genes andgenes the ITS1-5.8S-ITS2and the ITS1-5.8S-ITS2 segments segmentsof the rDNA of the repeats) rDNA identities repeats)/similarities. identities/similaritie The generals. The practice general of sequence-based practice of sequence-based strain identification strain identificationis a search with is thea search sequence with of the the sequence strain in of nucleotide the strain databases in nucleotide for identical databases/similar for identical/similar sequences and sequencesassigning theand strain assigning to the the species strain whoseto the databasespecies whose sequence database is found sequence most similar.is found Themost sequence similar. Theof the sequence strain is of then the routinely strain is deposited then routinely in the databasedeposited (most in the journals database request (most accession journals numbers) request accessionunder this numbers) taxonomic under name this usually taxonomic without name an expert usually taxonomic without verification.an expert taxonomic Since small verification. sequence Sincedifferences small are sequence usually tolerateddifferences during are usually identification, tolerated the newduring entries identification, will gradually the fillnew up entries the barcode will graduallygaps separating fill up thethe closely barcode related gaps species;separating the the species closely boundaries related species; gradually the become species fuzzy. boundaries Thus, graduallythe taxonomic become identification fuzzy. Thus, of new the isolates taxonomic by comparing identification their rDNAof new sequences isolates withby comparing those deposited their rDNAin databases sequences can with easily those lead deposited to false results. in databases In addition can easily to this lead general to false problem, results. In other addition diffi cultiesto this Microorganisms 2020, 8, 1029 3 of 19 can also arise when pulcherrimin-producing Metschnikowia strains are to be identified taxonomically. The results of the in-depth analyses of the rDNA repeats of certain type strains [13,14], the hybridization of type strains with each-other [14] and the analysis of genome sequences (e.g., [15–17]) raised doubts as to whether the taxonomic division of the M. pulcherrima clade is correct at all. The incongruences around the mechanism of the antimicrobial antagonism pose another problem. While many researchers associate it with iron depletion, others prefer the view that non-iron-related mechanisms similar to those known in other antagonistic microorganisms are also involved or even play the major role. This review seeks
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