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      Microorganisms in Fermented Apple Beverages: Current Knowledge and Future Directions

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          Abstract

          Production of fermented apple beverages is spread all around the world with specificities in each country. ‘French ciders’ refer to fermented apple juice mainly produced in the northwest of France and often associated with short periods of consumption. Research articles on this kind of product are scarce compared to wine, especially on phenomena associated with microbial activities. The wine fermentation microbiome and its dynamics, organoleptic improvement for healthy and pleasant products and development of starters are now widely studied. Even if both beverages seem close in terms of microbiome and process (with both alcoholic and malolactic fermentations), the inherent properties of the raw materials and different production and environmental parameters make research on the specificities of apple fermentation beverages worthwhile. This review summarizes current knowledge on the cider microbial ecosystem, associated activities and the influence of process parameters. In addition, available data on cider quality and safety is reviewed. Finally, we focus on the future role of lactic acid bacteria and yeasts in the development of even better or new beverages made from apples.

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          Most cited references149

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          Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera

          Lactobacilli are a diverse group of species that occupy diverse nutrient-rich niches associated with humans, animals, plants and food. They are used widely in biotechnology and food preservation, and are being explored as therapeutics. Exploiting lactobacilli has been complicated by metabolic diversity, unclear species identity and uncertain relationships between them and other commercially important lactic acid bacteria. The capacity for biotransformations catalysed by lactobacilli is an untapped biotechnology resource. Here we report the genome sequences of 213 Lactobacillus strains and associated genera, and their encoded genetic catalogue for modifying carbohydrates and proteins. In addition, we describe broad and diverse presence of novel CRISPR-Cas immune systems in lactobacilli that may be exploited for genome editing. We rationalize the phylogenomic distribution of host interaction factors and bacteriocins that affect their natural and industrial environments, and mechanisms to withstand stress during technological processes. We present a robust phylogenomic framework of existing species and for classifying new species.
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            Yeast interactions and wine flavour.

            Wine is the product of complex interactions between fungi, yeasts and bacteria that commence in the vineyard and continue throughout the fermentation process until packaging. Although grape cultivar and cultivation provide the foundations of wine flavour, microorganisms, especially yeasts, impact on the subtlety and individuality of the flavour response. Consequently, it is important to identify and understand the ecological interactions that occur between the different microbial groups, species and strains. These interactions encompass yeast-yeast, yeast-filamentous fungi and yeast-bacteria responses. The surface of healthy grapes has a predominance of Aureobasidium pullulans, Metschnikowia, Hanseniaspora (Kloeckera), Cryptococcus and Rhodotorula species depending on stage of maturity. This microflora moderates the growth of spoilage and mycotoxigenic fungi on grapes, the species and strains of yeasts that contribute to alcoholic fermentation, and the bacteria that contribute to malolactic fermentation. Damaged grapes have increased populations of lactic and acetic acid bacteria that impact on yeasts during alcoholic fermentation. Alcoholic fermentation is characterised by the successional growth of various yeast species and strains, where yeast-yeast interactions determine the ecology. Through yeast-bacterial interactions, this ecology can determine progression of the malolactic fermentation, and potential growth of spoilage bacteria in the final product. The mechanisms by which one species/strain impacts on another in grape-wine ecosystems include: production of lytic enzymes, ethanol, sulphur dioxide and killer toxin/bacteriocin like peptides; nutrient depletion including removal of oxygen, and production of carbon dioxide; and release of cell autolytic components. Cell-cell communication through quorum sensing molecules needs investigation.
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              A renaissance for the pioneering 16S rRNA gene.

              Culture-independent molecular surveys using the 16S rRNA gene have become a mainstay for characterizing microbial community structure over the past quarter century. More recently this approach has been overshadowed by metagenomics, which provides a global overview of a community's functional potential rather than just an inventory of its inhabitants. However, the pioneering 16S rRNA gene is making a comeback in its own right thanks to a number of methodological advancements including higher resolution (more sequences), analysis of multiple related samples (e.g. spatial and temporal series) and improved metadata, and use of metadata. The standard conclusion that microbial ecosystems are remarkably complex and diverse is now being replaced by detailed insights into microbial ecology and evolution based only on this one historically important marker gene.
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                Author and article information

                Journal
                Microorganisms
                Microorganisms
                microorganisms
                Microorganisms
                MDPI
                2076-2607
                25 July 2017
                September 2017
                : 5
                : 3
                : 39
                Affiliations
                Aliments Bioprocédés Toxicologie Environnements, Normandie Univ., UNICAEN, UNIROUEN, 14000 Caen, France; fabien.cousin@ 123456unicaen.fr (F.J.C.); rozenn.leguellec@ 123456unicaen.fr (R.L.G.); margot.schlusselhuber@ 123456unicaen.fr (M.S.); marion.dalmasso@ 123456unicaen.fr (M.D.); jean-marie.laplace@ 123456unicaen.fr (J.-M.L.)
                Author notes
                [* ]Correspondence: marina.cretenet@ 123456unicaen.fr ; Tel: +33-231-565-785
                Author information
                https://orcid.org/0000-0001-6874-387X
                https://orcid.org/0000-0003-1875-2748
                Article
                microorganisms-05-00039
                10.3390/microorganisms5030039
                5620630
                28757560
                735cbff6-4efe-407a-a05f-f2a05aceb386
                © 2017 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 27 June 2017
                : 21 July 2017
                Categories
                Review

                apple,cider,lactic acid bacteria,fermentation,organoleptic quality,safety improvement,microbial diversity

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