PUBLISHED: 29 MARCH 2016!| ARTICLE NUMBER: 16039 | DOI: 10.1038/NMICROBIOL.2016.39 feature Artisanal food microbiology Arielle J. Johnson

Because of their ability to biochemically transform their growing environments, microorganisms are playing a new creative role as a culinary tool, enabling both professional and amateur cooks to create entirely new flavours from existing ingredients.

he use of fermentation — loosely defned as the transformation of Tfood by microorganisms — as a means of preserving food goes back thousands of years, if not further. Carefully controlled fermentation processes are key to elaborate well-known delicacies whose culinary absence would be sorely felt, such as cheese, chocolate, , wine, cofee, bread, , yogurt, beer and pickles. Fermentation and cuisine have a long, well-cemented relationship all over the world (Box 1), but for the most part, these processes have been confned to specialized workshops, such as at a soy sauce producer or vinegar houses, rather than the day-to-day workings of the restaurant kitchen. While it’s increasingly common for restaurants to ofer high-quality bread, made in-house from a purposefully cultivated sourdough starter, the same has not been true of other fermented products that appear on the menu. ARIELLE JOHNSON Tat is, until recently, when cooks around Figure 1 | Arielle Johnson in a soy sauce factory in Saitama, Japan. the world have begun to discover (or, more accurately, to rediscover, drawing from history and other cultures) the possibilities organisms — what one might call ‘culinary kitchen, practically the only time you make of using fermentation processes in the microorganisms’ — are bacteria and fungi. new favour molecules while cooking is kitchen. Call it a revival, a natural outgrowth Lactic acid bacteria (LAB) of the genii through the breakdown and caramelization of the ‘do-it-yourself’ mentality, or artisanal Lactobacillus, Leuconostoc, Pediococcus of sugars by heat, or through the similarly food microbiology; a new appreciation and Lactococcus, produce lactic acid from heat-driven Maillard reaction. Tis process for old techniques and a reinterpretation sugars in products like sauerkraut, kimchi, creates the favours of baked bread and of their uses is transforming the human– yogurt, cheese and miso. Acetic acid roasted meat through the reduction of microorganism–substrate relationship into bacteria (AAB), obligate anaerobes in the sugars and free amino acids. Meat may be a new cooking tool, every bit as essential as family Acetobacteraceae, are responsible aged to develop new favours by allowing a paring knife or frying pan. It is giving chefs for the creation of vinegar. Te yeast endogenous proteases in the animal’s cells new methods for working in concert with Saccharomyces cerevisiae metabolizes to slowly break down proteins and release bacteria and fungi to transform ingredients sugar into ethyl alcohol and carbon in amino acids. Generally, however, the and create new favours. wine, beer and bread, and the salt-tolerant creation of favour molecules occurs at the Microorganisms live in or on their food Zygosaccharomyces rouxii contributes farm, during the process of growing and source, and biochemically transform it to to the toasty, malty favour of soy sauce rearing plants and animals. In the kitchen, extract energy, producing metabolites in (Fig. 1). Useful moulds include Aspergillus the work becomes the preservation, the process. In general, a pool of larger- oryzae, whose amylolytic and proteolytic capture, and rearrangement of these molecular-weight, and usually less favour- activities on grains constitute the building favours through the controlled application active molecules —like starches, sugars, blocks for , miso, and soy sauce; and of heat, and generally avoids microbial proteins, and alcohol — are transformed Penicillium roqueforti, which creates the processes, which would commonly be into a more diverse group of tastier, smaller blue-green veins (and pungent favour) of considered to be spoilage. Fermenting for molecules, such as amino acids, organic blue cheeses. favour has not traditionally been an area acids, esters, sugars, alcohols, and aromatic When you ferment something, you of interest for cooks, but adding microbial compounds. Te most commonly used create favour. In a traditional Western transformation to their repertoire can give

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Other established restaurants have Box 1 | Cuisinology. also drawn inspiration for their cuisine from working with microorganisms. . Smoked, dried, fermented Kosho. Short for yuzukosho, a fermented Sean Brock’s restaurant, Husk, takes a tuna that is shaved and steeped with kelp mixture of citrus peel, chilli peppers similar geographic approach to creative to make , one of the basic broths of and salt, a specialty of the Kyushu region limitation, using only ingredients . of Japan. from south of the Mason–Dixon line. Tis means that to put olive oil on his Kefr. A LAB–yeast mixed culture dairy Kvass. A beet- or rye-bread-based menu, he had to fnd a grower in Texas. fermentation originating in the Caucasus fermented beverage popular in Baltic and Combined with childhood inspiration mountain region. Slavic cultures. from Brock’s grandmother, who would ferment sauerkraut, sour corn and Koji. Aspergillus oryzae mould inoculated Miso. A two-stage fermentation technique wines, it also lead to collard greens and grown on grains or legumes, from Japan; the frst stage traditionally uses fermented in the style of sauerkraut, traditionally , barley or soybeans. rice, barley, or soybean koji. In the second fermented peppers and a ‘vinegar pantry’ Koji is the Japanese name; the process stage, salt and soybeans are added and with vinegars made from strawberries, originated in the Neolithic period in China secondary lactic fermentation takes place, sorghum and, infamously, Mountain where it was called qu or chhü. Koji is rich yielding a rich, sweet, tangy, salty, and Dew. Likewise, the New York restaurant in amylases and proteases, which makes -favoured paste. group Momofuku has a lab devoted to it useful as a catalyst for making other developing new food techniques, and fermented products like miso, soy sauce Tempeh. A cake-like soybean fermentation has devised fermentations inspired by and sake. from Indonesia made using moulds in the Japanese miso and katsuobushi, but made genus Rhizopus. with locally-sourced pork, spelt and Kombucha. An acidic liquid or beverage chickpeas. Bar Tartine in San Francisco, made from fermenting sweetened tea . Japanese term for pickles. helmed by chefs Nicolaus Balla and with a mixed culture of yeasts and acetic Styles include kasuzuke, (pickling with Cortney Burns, features a regular rotation bacteria that form a pellicle or zoogloeal kasu, lefover sake lees); misozuke of lacto-fermented vegetables on its menu, mat. Te origin of kombucha is unclear, (pickling in miso); nukazuke (pickling in with koji ofen making an appearance though Russia, China, Japan and Korea are a bed of nuka, rice bran); and shiozuke, along with a spectrum of fermented all contenders. (pickling in salt). beverages including dairy and water kefr and kvass, all of which are produced in-house. Restaurants have not limited them a new dimension of control over for exactly the species of yeast, bacteria and their creative use of microorganisms to favour, and new avenues for expressing the moulds that we use to make misos, vinegars, fermentation alone — many algae strains, potential of their ingredients. lactic fermentations, kombuchas and other known for their oceanic favours — have As a favour chemist, for the last products (see Box 1). In-house fermented been featured in dishes at Number 9 Park several years I’ve worked on collaborative products play a role in nearly every dish in Boston and Aponiente in Spain, and research with kitchens and restaurants to at noma. Fermentation has become vital better understand the inter-relationship to the menu (as well as to those of many of food and science. In my job as head of other restaurants), because of its ability to research at MAD (a food culture nonproft transform and create favours. Consider and symposium with a close relationship acidity — you might add this to a dish in to restaurant noma in Copenhagen) I the form of lemon juice, or perhaps wine have a broad mandate to use a variety of vinegar, but rule out citrus and grapes, approaches and tools to help all cooks better neither of which thrive in a Scandinavian understand food. Te cuisine of noma climate, and your options are fairly limited. is based around geographical limitation: Turning to the world of microorganisms, ingredients must come (mostly) from the several types of bacteria produce acids Nordic region. As with many limitations, as their primary metabolite, chiefy LAB this has led to a blossoming of gastronomic and AAB. Lars Williams, noma’s head of creativity in the search for favours, with R&D and my lab partner, has spent much fermentation at its heart. My job there is of the last decade developing, exploring to distil technical and scholarly knowledge and iterating these techniques, ‘dialling- from many diferent felds into practical in’ subtle diferences in the quality of knowledge that any cook can use. their acidity and its balance with other Most of our lab is dedicated to favours from the substrate or from fermentation, both development and parallel fermentation products. A dish at production. Inside modifed shipping noma might get its acidity from a favour containers, which we retroftted ourselves, palette that includes fruity and foral wild are seven rooms that function as climate- chamomile kombucha, earthy and tangy AND NOMA ARIELLE JOHNSON controlled incubators, able to hold lacto-fermented mushrooms, a caramelized temperatures between –30°C and 60°C, and and robust reduction of rye miso, and clean Figure 2 | A conceptual recipe for ‘squid garum’, humidity levels of up to 99%. Tis makes it and creamy lactic fermentation of barley a fish-sauce-like product made with squid ofcuts possible to create hospitable environments koji (Fig. 2). and koji.

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lichens, which are symbiotic growths of Duluth, Minnesota, is a woodworker by fungi with algae or cyanobacteria (such as trade who specializes in handmade food reindeer moss — which is only colloquially and fermentation tools like cedar trays and called a moss) are frequently found on boxes for making koji, as well as oak and Scandiavian tasting menus. cedar barrels for aging soy sauces and beers One of the drivers of the recent under the label ‘Decadence by Hand’. He fermentation renaissance is writer and also teaches smoking, wild foods, butchery ‘fermentation revivalist’ Sandor Katz. and charcuterie. On Facebook, groups like Katz began fermenting vegetables in the Fermenter’s Kitchen and Wild Fermentation early nineties, when he found himself are a constantly expanding resource of with too many cabbages on his hands, and experiments and expertise, all freely shared. realized they could be made into sauerkraut, Within certain technical boundaries — something that central Europeans know like measuring and using the correct amount all too well. From sauerkraut — which he of salt in lactic fermentations; ensuring is enthused about to the point of being that air gets into a vinegar fermentation nicknamed Sandor Kraut — he moved on and stays out of a wine fermentation; that to making his own yogurt, cheese, wines, ARIELLE JOHNSON Aspergillus oryzae fermentations stay in a sourdough and eventually more technically Figure 3 | Rice koji in handmade cedar koji trays at 30–35 °C temperature range; and a healthy challenging mould-derived fermentations a miso kura in Nasu, Japan. respect for the low-air, low-acid, low-salt, like koji, miso and tempeh. Katz has taught high-protein conditions that could foster these techniques since 1998, and his three botulism — there’s a huge territory ripe books — Wild Fermentation; Te Revolution Te available knowledge base is deep for experimentation and discovery, if one Will Not Be Microwaved; and Te Art but scattered and ad hoc. Given that the is not afraid of failing and trying again. It’s of Fermentation — are frequently cited processes involved take weeks or months possible to begin experimenting with lactic as essential resources and are found on to complete and vary widely depending fermentation with limited investments in restaurants’ reference bookshelves around on the local microfora, ingredient salt, a container, and a weight; to begin the world. composition, temperature, humidity and making miso, more self-education and trial Berkeley, California is home to many other parameters; experimentation, and error in the technical temperature- another fermentation institution, the trial and error, discovery and self- control aspects of growing koji are required. Cultured Pickle Shop, owned and run by education go hand in hand with making Functional thinking about the chemical Alex Hozven and Kevin Farley, who began this happen. All four are in evidence on makeup of substrates can enable new fermenting miso when they were living of social media feeds, with Instagram, the discoveries — the lacto-fermentability of the grid in Mendocino County, California photo-sharing mobile app, acting as a kind mushrooms, or the possibility of making a in the mid-nineties. Tey were able to of peer-reviewed forum of ideas for cooks miso not with the traditional soybeans, but source Aspergillus oryzae spores from a (check out @teamsilent, @tmgastronaut, with yellow peas, chickpeas, or spent brewer’s serendipitously nearby company called @ericedgin, @culturedpickleshop, malt — and new ideas can come from GEM Cultures, then the only domestic @joshfratoni, @momofukulab, as well as unexpected sources, like patent flings on fsh supplier of koji moulds in the US, which @lars_williams and @arielle_johnson for sauce processing, conference proceedings is still in operation and has provisioned some good examples). Young chefs like on ethnobiology, historical books on science many experimental fermenters with their Jason White at Emmer & Rye in Austin, and civilization in China, or chemical frst supplies of spores. In the twenty-plus and Ryan Poli at the Catbird Seat in engineering papers on the enzymatic activity years since, the couple’s repertoire has Nashville, are applying these ideas to their of fungi. Successful exploration in artisan expanded vastly. Today, it encompasses local terroir, drawing inspiration from microbiology requires a taste for self- many diferent styles of lactic fermentation ancient techniques, their own childhood education and empiricism, as well as what and sauerkraut, fruit- and herb-enhanced experiences with farm fermentation, and can best be described as a cultivated intuition kombuchas, and variations on the time spent at other restaurants around or knack, making for a skillset somewhere traditional Japanese pickling styles called the world, building up their own research between craf and science. tsukemono, including kasuzuke, misozuke libraries, while sharing their own fndings Where science applied creatively to food and nukazuke (Box 1). Although it’s almost publicly for others to fnd. is concerned, microbiology and microbial impossible to get their products outside the Fermentation ofen goes hand-in-hand ecology are joining an ever-expanding list, San Francisco Bay Area and, in some cases, with other hands-on food preparations matured over the past seven or eight years, outside of their shop (wild inoculated, such as butchery, foraging wild foods, and of new, more critical ways of exploring unpasteurized fermentations don’t ship other practices that extend the boundaries cuisine. An evolution from the ‘molecular well), their infuence has extended much of ‘cooking,’ beyond the traditional sense gastronomy’ formulated in the 1990s, this further afeld. Singular products like citrus of preparing dishes. Tis is true for movement now touches on and draws koshos, burdock misozuke and watermelon restaurants — the overall use of foraged inspiration from agronomy, plant science, rind kasuzuke make them a popular wild herbs, fruits, fowers, and other plants favour chemistry, psychology, ethnobotany insider inspiration and an in-demand at noma is perhaps even more extensive and others. It’s going to be exciting (and, collaborator for chefs in California, Japan than that of fermentation — and also, hopefully, delicious) to see where the next and elsewhere. increasingly, for adventurous amateur cooks set of developments takes us. ❐ In the midst of all of this innovation, as well. Tere is a diverse and thriving home many young cooks and new restaurants fermentation scene, frequently cultivated Arielle J. Johnson is at MAD, c/o noma, are taking it as a given that fermentation alongside other DIY skills like pottery and Strandgade 93, 1401 Copenhagen K, Denmark. will have some place in their kitchens. woodworking (Fig. 3). Eric Edgin, from e-mail: [email protected]

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