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Journal ArticleDOI

Primary souring: A novel bacteria-free method for sour beer production.

01 Apr 2018-Food Microbiology (Food Microbiol)-Vol. 70, pp 76-84

TL;DR: A new LAB-free paradigm for sour beer production is suggested that is term "primary souring" because the lactic acid production and resultant pH decrease occurs during primary fermentation, as opposed to kettle souring or souring via mixed culture fermentation.
Abstract: In the beverage fermentation industry, especially at the craft or micro level, there is a movement to incorporate as many local ingredients as possible to both capture terroir and stimulate local economies. In the case of craft beer, this has traditionally only encompassed locally sourced barley, hops, and other agricultural adjuncts. The identification and use of novel yeasts in brewing lags behind. We sought to bridge this gap by bio-prospecting for wild yeasts, with a focus on the American Midwest. We isolated 284 different strains from 54 species of yeast and have begun to determine their fermentation characteristics. During this work, we found several isolates of five species that produce lactic acid and ethanol during wort fermentation: Hanseniaspora vineae, Lachancea fermentati, Lachancea thermotolerans, Schizosaccharomyces japonicus, and Wickerhamomyces anomalus. Tested representatives of these species yielded excellent attenuation, lactic acid production, and sensory characteristics, positioning them as viable alternatives to lactic acid bacteria (LAB) for the production of sour beers. Indeed, we suggest a new LAB-free paradigm for sour beer production that we term "primary souring" because the lactic acid production and resultant pH decrease occurs during primary fermentation, as opposed to kettle souring or souring via mixed culture fermentation.
Topics: Souring (60%), Fermentation (58%), Brewing (53%)

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1
Primary souring: a novel bacteria-free method for sour beer production 1
Kara Osburn
a
, Justin Amaral
b
, Sara R. Metcalf
a
, David M. Nickens
a
, Cody M. Rogers
a
, 2
Christopher Sausen
a
, Robert Caputo
c
, Justin Miller
c
, Hongde Li
d
, Jason M. Tennessen
d
, and 3
Matthew L. Bochman
a,c*
4
a
Molecular and Cellular Biochemistry Department, 212 South Hawthorne Drive, Simon Hall 5
MSB1, room 405B, Indiana University, Bloomington, IN 47405, USA. 6
klosburn@umail.iu.edu
7
srmetcal@indiana.edu
8
dnickens@indiana.edu
9
codroger@indiana.edu
10
csausen@indiana.edu
11
bochman@indiana.edu
12
13
b
Mainiacal Brewing Company, Bangor, ME 04401, USA. 14
jamaral@mainiacalbrewingcompany.com
15
16
c
Wild Pitch Yeast, Bloomington, IN 47405, USA. 17
rob@drinkin.beer
18
justin@blackacrebrewing.com
19
20
d
Department of Biology, Indiana University, 1001 East Third Street, Bloomington, IN 47405, 21
USA. 22
hongde.li@hotmail.com
23
jtenness@indiana.edu
24
25
*
Corresponding author: 26
Matthew L. Bochman, Ph.D. 27
Assistant Professor 28
Molecular and Cellular Biochemistry Department 29
212 South Hawthorne Drive 30
Simon Hall MSB1, room 405B 31
Indiana University 32
bochman@indiana.edu
33
812-856-2095 34
.CC-BY-NC-ND 4.0 International licensea
certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under
The copyright holder for this preprint (which was notthis version posted July 28, 2017. ; https://doi.org/10.1101/121103doi: bioRxiv preprint

2
Abstract 35
In the beverage fermentation industry, especially at the craft or micro level, there is a movement 36
to incorporate as many local ingredients as possible to both capture terroir and stimulate local 37
economies. In the case of craft beer, this has traditionally only encompassed locally sourced 38
barley, hops, and other agricultural adjuncts. The identification and use of novel yeasts in 39
brewing lags behind. We sought to bridge this gap by bio-prospecting for wild yeasts, with a 40
focus on the American Midwest. We isolated 284 different strains from 54 species of yeast and 41
have begun to determine their fermentation characteristics. During this work, we found several 42
isolates of five species that produce lactic acid and ethanol during wort fermentation: 43
Hanseniaspora vineae, Lachancea fermentati, Lachancea thermotolerans, Schizosaccharomyces 44
japonicus, and Wickerhamomyces anomalus. Tested representatives of these species yielded 45
excellent attenuation, lactic acid production, and sensory characteristics, positioning them as 46
viable alternatives to lactic acid bacteria (LAB) for the production of sour beers. Indeed, we 47
suggest a new LAB-free paradigm for sour beer production that we term “primary souring48
because the lactic acid production and resultant pH decrease occurs during primary fermentation, 49
as opposed to kettle souring or souring via mixed culture fermentation. 50
51
Keywords: yeast, lactic acid, sour beer, heterolactic fermentation 52
Chemical compounds studied in this article: 53
Lactic acid (PubChem CID: 612); Ethanol (PubChem CID: 702) 54
Abbreviations: ABV, alcohol by volume; DIC, differential interference contrast; EtOH, ethanol; 55
FG, final gravity; gDNA, genomic DNA; IBU, international bittering unit; LAB, lactic acid 56
.CC-BY-NC-ND 4.0 International licensea
certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under
The copyright holder for this preprint (which was notthis version posted July 28, 2017. ; https://doi.org/10.1101/121103doi: bioRxiv preprint

3
bacteria; LASSO, lactic acid specific soft-agar overlay; N-J, neighbor-joining; OG, original 57
gravity; WLN, Wallerstein Laboratories nutrient; YPD, yeast extract, peptone, and dextrose 58
59
.CC-BY-NC-ND 4.0 International licensea
certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under
The copyright holder for this preprint (which was notthis version posted July 28, 2017. ; https://doi.org/10.1101/121103doi: bioRxiv preprint

4
1. Introduction 60
Currently, we are in the midst of a global craft beer boom, with the number of small 61
independent breweries growing at a tremendous pace (1). This has led to increased competition, 62
not only with the large macrobrewers but among the craft brewers themselves. As such, there is a 63
need in the industry to differentiate oneself from, minimally, other local breweries. This has 64
fueled experimentation with the core beer ingredients of water (2), malted grain (3), hops (4) and 65
yeast (5), as well as with various adjuncts. Much of this experimentation is also focused on 66
locally sourced ingredients to capture terroir and bolster the local economy (6,7). 67
Despite this widespread experimentation, the isolation and use of novel yeasts for 68
brewing has lagged behind that of the other ingredients. This is in part due to the easy 69
availability of numerous ale and lager strains from reputable commercial suppliers such as White 70
Labs, Wyeast, and Lallemand (8). However, focusing on two species, Saccharomyces cerevisiae 71
for ales and Saccharomyces pastorianus for lagers, naturally limits the genotypic and phenotypic 72
variation available in brewing strains. This also translates into a limited palette of aromatic and 73
flavor compounds made by these strains, especially considering their extremely high 74
evolutionary relatedness (9,10). 75
To overcome this constraint, several laboratories and breweries have begun to culture 76
wild yeasts and characterize their beer fermentation capabilities. Most efforts have focused on 77
wild ale and lager strains (11,12) to increase the available genetic diversity of strains that 78
naturally display high ethanol tolerance. However, multiple strains of yeasts in the 79
Brettanomyces, Hanseniaspora, Lachancea, and Pichia genera (13-15) have also been 80
investigated as alternative species for the production of beer. 81
.CC-BY-NC-ND 4.0 International licensea
certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under
The copyright holder for this preprint (which was notthis version posted July 28, 2017. ; https://doi.org/10.1101/121103doi: bioRxiv preprint

5
We also recently began bio-prospecting for wild yeasts with desirable brewing 82
characteristics (5). Here, we report the collection of nearly 300 strains from 26 genera. During 83
trial wort fermentations, we found that strains from five species (Hanseniaspora vineae, 84
Lachancea fermentati, Lachancea thermotolerans, Schizosaccharomyces japonicus, and 85
Wickerhamomyces anomalus) were capable of heterolactic fermentation of sugar into lactic acid, 86
ethanol, and CO
2
. Larger-scale brewing with four strains demonstrated that these yeasts are 87
highly attenuative, flocculate well, yield appreciable levels of lactic acid, and produce pleasant 88
aromatic and flavor compounds. We suggest a new paradigm for sour beer production called 89
“primary souring” that avoids the use of lactic acid bacteria (LAB) and instead relies solely on 90
lactic acid production by a heterofermentative yeast during primary fermentation. 91
92
2. Materials and methods 93
2.1. Strains, media, and other reagents 94
S. cerevisiae strain WLP001 was purchased from White Labs (San Diego, CA). Wild 95
strains were isolated as described in (5). All yeast strains were routinely grown on yeast extract, 96
peptone, and dextrose (YPD; 1% (w/v) yeast extract, 2% (w/v) peptone, and 2% (w/v) glucose) 97
plates containing 2% (w/v) agar at 30°C and in YPD liquid culture at 30°C with aeration unless 98
otherwise noted. All strains were stored as 15% (v/v) glycerol stocks at -80°C. Media 99
components were from Fisher Scientific (Pittsburgh, PA, USA) and DOT Scientific (Burnton, 100
MI, USA). All other reagents were of the highest grade commercially available. 101
2.2. Strain identification and phylogenetic analysis 102
.CC-BY-NC-ND 4.0 International licensea
certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under
The copyright holder for this preprint (which was notthis version posted July 28, 2017. ; https://doi.org/10.1101/121103doi: bioRxiv preprint

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TL;DR: 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.
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825 citations


"Primary souring: A novel bacteria-f..." refers background in this paper

  • ...Although yeasts in the Hansenia genus are the predominant species found on grapes (Fleet, 2003; Jolly et al., 2014; Swiegers and Pretorius, 2005), they are also found elsewhere (reviewed in (Lappe-Oliveras et al....

    [...]

  • ...Although yeasts in the Hansenia genus are the predominant species found on grapes (Fleet, 2003; Jolly et al., 2014; Swiegers and Pretorius, 2005), they are also found elsewhere (reviewed in (Lappe-Oliveras et al., 2008))....

    [...]


Journal ArticleDOI
M.G. Lambrechts1, Isak S. Pretorius1Institutions (1)
TL;DR: The importance of untapping the hidden wealth of indigenous yeast species present on grapes, and the selection and genetic development of yeast starter culture strains with improved flavour profiles are highlighted.
Abstract: The most mysterious aspect of wine is the endless variety of flavours that stem from a complex, completely non-linear system of interactions among many hundreds of compounds. In its widest sense, wine flavour refers to the overall impression of both aroma and taste components. Aroma is usually associated with odorous, volatile compounds; the bouquet of wine refers to the more complex flavour compounds which evolve as a result of fermentation, elevage and ageing. With the exception of terpenes in the aromatic grape varieties and alkoxypyrazines in the herbaceous cultivars, perceived flavour is the result of absolute amounts and specific ratios of many of these interactive compounds, rather than being attributable to a single "impact" compound. Without underestimating the complexity of these interactive effects or negating the definitive role played by the accumulated secondary grape metabolites in the varietal character of wine, this review will focus mainly on the contribution of yeast fermentation to the sensorial quality of the final product. Yeast and fermentation conditions are claimed to be the most important factors influencing the flavours in wine. Both spontaneous and inoculated wine fermentations are affected by the diversity of yeasts associated with the vineyard and winery. During the primary alcoholic fermentation of sugar, the wine yeast, Saccharomyces cerevisiae, together with other indigenous non-Saccharomyces species, produce ethanol, carbon dioxide and a number of by-products. Of these yeast-derived metabolites, the alcohols, acetates and C4-C8 1tfatty acid ethyl esters are found in the highest concentration in wine. While the volatile metabolites contribute to the fermentation bouquet ubiquitous to all young wines, the production levels of these by-products are variable and yeast strain specific. Therefore, this article also highlights the importance of untapping the hidden wealth of indigenous yeast species present on grapes, and the selection and genetic development of yeast starter culture strains with improved flavour profiles. In the future, some winemakers may prefer to use mixtures of indigenous yeast species and tailored S. cerevisiae strains as starter cultures to reflect the biodiversity and stylistic distinctiveness of a given region. This will help winemakers to fullfil the consumer's demand for individual wines with intact local character and to ensure the survival of wine's most enthralling aspect - its endless variety.

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"Primary souring: A novel bacteria-f..." refers background in this paper

  • ..., 2004), wine production (Lambrechts and Pretorius, 2000), and was isolated from spontaneously fermented beer in North Carolina (Woodward, 2013)....

    [...]

  • ...…associated with indigenous fermented beverages (e.g., kaffir beer, plantain beer, palm wine, sugar cane wine, and sake) around the world (Josephsen et al., 2004), wine production (Lambrechts and Pretorius, 2000), and was isolated from spontaneously fermented beer in North Carolina (Woodward, 2013)....

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TL;DR: The phylogeny and timescale of life are becoming better understood as the analysis of genomic data from model organisms continues to grow and the emphasis on historical patterns is helping to bridge barriers among organism-based research communities.
Abstract: The phylogeny and timescale of life are becoming better understood as the analysis of genomic data from model organisms continues to grow. As a result, discoveries are being made about the early history of life and the origin and development of complex multicellular life. This emerging comparative framework and the emphasis on historical patterns is helping to bridge barriers among organism-based research communities.

771 citations


"Primary souring: A novel bacteria-f..." refers background in this paper

  • ..., YH156) occurring approximately 1 billion years ago (Hedges, 2002)....

    [...]

  • ...vineae, which are separated by ~1 billion years of evolution (Hedges, 2002), may indicate that heterolactic fermentation is an ancient and conserved metabolic process among single-celled fungi....

    [...]

  • ...…related to ale yeast (WLP001), but the other two (S. japonicus, andW. anomalus) formmore distinct clades, with the divergence between budding yeasts such as S. cerevisiae (e.g., WLP001) and fission yeasts such as S. japonicus (e.g., YH156) occurring approximately 1 billion years ago (Hedges, 2002)....

    [...]

  • ...…ethanol-tolerant yeasts, but its presence in the fission yeast S. japonicus and budding yeasts like H. vineae, which are separated by ~1 billion years of evolution (Hedges, 2002), may indicate that heterolactic fermentation is an ancient and conserved metabolic process among single-celled fungi....

    [...]


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TL;DR: This article reviews the specific flavour-active characteristics of those non-Saccharomyces species that might play a positive role in both spontaneous and inoculated wine ferments and raises important questions about the direction of mixed-fermentation research to address market trends regarding so-called 'natural' wines.
Abstract: Saccharomyces cerevisiae and grape juice are ‘natural companions’ and make a happy wine marriage. However, this relationship can be enriched by allowing ‘wild’ non- Saccharomyces yeast to participate in a sequential manner in the early phases of grape must fermentation. However, such a triangular relationship is complex and can only be taken to ‘the next level’ if there are no spoilage yeast present and if the ‘wine yeast’ – S. cerevisiae – is able to exert its dominance in time to successfully complete the alcoholic fermentation. Winemakers apply various ‘matchmaking’ strategies (e.g. cellar hygiene, pH, SO2, temperature and nutrient management) to keep ‘spoilers’ (e.g. Dekkera bruxellensis ) at bay, and allow ‘compatible’ wild yeast (e.g. Torulaspora delbrueckii, Pichia kluyveri, Lachancea thermotolerans and Candida/Metschnikowia pulcherrima ) to harmonize with potent S. cerevisiae wine yeast and bring the best out in wine. Mismatching can lead to a ‘two is company, three is a crowd’ scenario. More than 40 of the 1500 known yeast species have been isolated from grape must. In this article, we review the specific flavour-active characteristics of those non- Saccharomyces species that might play a positive role in both spontaneous and inoculated wine ferments. We seek to present ‘single-species’ and ‘multi-species’ ferments in a new light and a new context, and we raise important questions about the direction of mixed-fermentation research to address market trends regarding so-called ‘natural’ wines. This review also highlights that, despite the fact that most frontier research and technological developments are often focussed primarily on S. cerevisiae , non- Saccharomyces research can benefit from the techniques and knowledge developed by research on the former.

529 citations


"Primary souring: A novel bacteria-f..." refers background in this paper

  • ...theromtolerans have been studied for their effects on wine fermentation (reviewed in (Jolly et al., 2014)), though usually in co-fermentations with S....

    [...]

  • ...Although yeasts in the Hansenia genus are the predominant species found on grapes (Fleet, 2003; Jolly et al., 2014; Swiegers and Pretorius, 2005), they are also found elsewhere (reviewed in (Lappe-Oliveras et al....

    [...]

  • ...Various strains of L. theromtolerans have been studied for their effects on wine fermentation (reviewed in (Jolly et al., 2014)), though usually in co-fermentations with S. cerevisiae (e.g., (Shekhawat et al., 2016; Benito et al., 2016)....

    [...]

  • ...Although yeasts in the Hansenia genus are the predominant species found on grapes (Fleet, 2003; Jolly et al., 2014; Swiegers and Pretorius, 2005), they are also found elsewhere (reviewed in (Lappe-Oliveras et al., 2008))....

    [...]


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