Cultured: How Ancient Foods Can Feed Our Microbiome

ALSO BY KATHERINE HARMON COURAGE

OCTOPUS: THE MOST MYSTERIOUS CREATURE IN THE SEA

an imprint of Penguin Random House LLC

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Copyright © 2019 by Katherine Harmon Courage

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Library of Congress Cataloging-in-Publication Data

Names: Courage, Katherine Harmon, author.

Title: Cultured : how ancient foods can feed our microbiome / Katherine Harmon Courage.

Description: New York : Avery, an imprint of Penguin Random House, [2019] | Includes bibliographical references and index.

Identifiers: LCCN 2018049621| ISBN 9781101905289 (hardcover) | ISBN 9781101905296 (ebook)

Subjects: LCSH: Food—Microbiology—Popular works.

Classification: LCC QR115 .C68 2019 | DDC 579/.16—dc23

LC record available at https://lccn.loc.gov/2018049621

p. cm.

Neither the publisher nor the author is engaged in rendering professional advice or services to the individual reader. The ideas, procedures, and suggestions contained in this book are not intended as a substitute for consulting with your physician. All matters regarding your health require medical supervision. Neither the author nor the publisher shall be liable or responsible for any loss or damage allegedly arising from any information or suggestion in this book.

Version_2

To my mom and dad, Pamela Rogers and William Harmon:

Thank you for encouraging me to ask lots of questions—and to get my hands dirty.

CONTENTS

ALSO BY KATHERINE HARMON COURAGE

TITLE PAGE

COPYRIGHT

DEDICATION

EPIGRAPH

INTRODUCTION

We Are Not Alone

CHAPTER ONE

Microbes: In Our Guts and Under Fire

CHAPTER TWO

What’s in the Gut

CHAPTER THREE

Feeding the Microbiome

CHAPTER FOUR

Quintessential Culture: Dairy

CHAPTER FIVE

Consider the Pickle: Produce

CHAPTER SIX

Intoxicating Ferments: Grains

CHAPTER SEVEN

Basic Beans: Legumes and Seeds

CHAPTER EIGHT

The Undead: Meat

CHAPTER NINE

Bringing It Home

CONCLUSION

Saving an Invisible World

FURTHER READING

ACKNOWLEDGMENTS

INDEX

ABOUT THE AUTHOR

I contain multitudes.

—WALT WHITMAN, SONG OF MYSELF, 1855

The dependence of the intestinal microbes on the food makes it possible to adopt measures to modify the flora in our bodies.

—ÉLIE METCHNIKOFF, THE PROLONGATION OF LIFE: OPTIMISTIC STUDIES, 1907

INTRODUCTION

•  •  •  •  •

We Are Not Alone

We enjoy seeing ourselves as the evolutionary apex, striding confidently, inevitably out of the primordial muck, descending from the trees, and perfecting our proud, upright posture.

I hate to be the bearer of humbling news, but we have not arrived at this perceived pinnacle alone. We’ve had help. I’m not talking about ancient apes or even the asteroid that wiped out the dinosaurs. I’m talking about bugs.

More precisely, we’ve had help from the trillions of bacteria, fungi, viruses, and archaea that have inhabited our bodies for millions of years—and had existed on this planet for billions of years before we even came along. Walt Whitman was more correct than he ever could have known. We contain multitudes beyond our wildest imaginations.

Not only do we contain these multitudes, but we also depend on them. Without our microbes, we wouldn’t be here. We would never develop properly functioning immune systems, we would not get many of the extra nutrients we need from food, and our whole bodies—inside and out—would be a vast, open, welcoming landscape for opportunistic pathogens to find a home. We would be dead meat.*

Recently we have not been doing these essential microbes any favors. Through our own passion for progress and scientific crudeness, and with a dash of hubris, we’ve actually been doing a fairly expeditious job ruining this complex and crucial bodily ecosystem. Our microbes, known collectively as the human microbiota or microbiome,* are disappearing.

This transformation is occurring just as we are beginning to learn about our microbes’ roles in health and disease. We are discovering links between changes in the microbiota and obesity, allergies, diabetes, and depression—all of which are currently soaring, despite our advances in medicine.

If we looked at our daily choices through the eyes of our microbes, it would appear as if we’ve been working systematically to make their lives and livelihoods difficult—if not impossible. It’s as if we’ve been on a blind rampage against some of our most important collaborators.

There are many ways in which we’ve stopped providing for—and in many cases, directly assaulted—our microbes. In just the past several generations, we have dramatically changed course from the vast majority of human history and prehuman evolution.

During this time, we have been waging a war on our microbes. For example, taking indiscriminate antibiotics* and, heck, just getting indoor plumbing, have upended our ancient microbiota in just the past handful of generations.* This assault has been a swift and efficient one—a cataclysmic extinction event in a matter of mere decades out of humans’ 200,000 years. Just seconds in our species’ day in the sun. And the vast health implications of this change are just beginning to dawn on us.

There is, however, another quietly powerful force acting on our microbiotas—a factor that has also veered wildly in recent generations. It is one that we are almost entirely in control of: diet.

Diet is in fact one of the most powerful ways we can influence our microbes. And we get to use it every day, multiple times. The thing is, never has what our species eats changed so quickly. Our great-grandmothers never tasted a drop of high-fructose corn syrup, let alone soda sweetened with sucralose. Several generations ago, there was no such thing as safe canning to preserve food. And for more than 99 percent of our species’ time on the planet, we were all hunter-gatherers by necessity. Even the most ancient of food innovations, the invention of agriculture, has happened in a proverbial blink of an evolutionary eye.

And we are now learning that most everything we eat—from probiotic yogurt to a serving of asparagus to a fatty pork chop—has an effect on our microbes, which in turn have an effect on us. And rapidly. What you eat for one meal can change the composition of your microbiome within twenty-four hours. Not only that, but it is also becoming clear that these microbes play a key role in translating our diet to health outcomes—good and bad.

•  •  •  •  •

Since the time of Galileo, it has been a slow move to stretch our minds away from the gravitational pull of the human-centric universe. The microbiome provides yet another mind-boggling reminder that we are neither masters of the cosmos, nor even truly masters of our own bodies.

For most of our history, unbeknownst to us, we gave our microbes food and shelter. They gave us protection from pathogens, extra available calories and vitamins, a well-tuned immune system, and possibly even mood regulation. Changes to our genes, environment, and diet were slow. Our microbes were able to adapt to us—and we could adapt to them.

It wasn’t a bad deal for either party. It is, after all, a two-way street of survival. Many species or strains of microbes have spent so long in the human gut (millennia upon millennia, getting passed along from generation to generation, back to our primate ancestors—and even beyond that) that it is the only place they can live. In other words, your microbes depend on you just as much as you depend on them. Perhaps more so. As a team of researchers noted in the journal Nature, The individualized microbiota of each person has a stake in his or her fitness. If we go, they go, individually and collectively. And no one wants to be out of a home or, worse yet, wiped out forever.

So what are we to do? We can never return ourselves to that ideal, microbially perfect past.* But that doesn’t mean we should ignore the results of thousands of generations’ dietary experimentation. After all, our human bodies and genes, for all they know, are still expecting the life and diet of our ancestors hundreds, if not thousands, of years ago. Without upending our contemporary lives and moving back to a lifestyle of preindustrial subsistence, we can start to pay a little more attention to that impactful role of diet.

As kimchi, kombucha, and kefir multiply on our market shelves, it behooves us to learn more about these foods—and where they fit into a traditional diet. Many of the store-bought fermented foods we encounter today bear but passing resemblance, nutritionally or microbially, to the traditional foods our ancestors made and consumed. And as we continue to refine our meals, we should examine the major roles whole and fibrous foods play in many traditional cuisines.

Furthermore, these foods did not develop in isolation. Just as we are learning about ourselves, it is also true that no food is an island. Each is part of a whole, diverse diet—full of vitamins, protein, and fiber. Learning about these foods in their local contexts—how they are prepared, what they are eaten with, and how people incorporate them into their daily lives—provides better insights into their use across cultures. It is unlikely, for example, that simply augmenting the standard American diet* with a bottle of kombucha is going to morph your physical or psychological health into that of a fit Buddhist monk. That one might even think such a thing remotely possible in the first place is a reminder that so many of us have our their traditional dietary compass (if you’ve ever felt adrift in an aisle of diet books, you will know yourself a fellow traveler).

This book is not here to prescribe the next fast track to weight loss or miracle health cure—in part because I do not believe such things truly exist and in part because the study of the gut microbiome is still in its infancy. Rather, it is a dip into the myriad ways we humans have found to nourish ourselves and our microbes. It is a discovery that we must consistently incorporate these foods into our diet. It is an urging to try new things and learn to love dirty, rough foods. It is a journey in discovering a disappearing palette of distinctive flavors and vanishing traditions of handmade* foods.

These foods bring with them sometimes-uncanny folk wisdom as well as flavors that even the most advanced industrial processes are hard-pressed to emulate.

To find the foods most teaming with microbial life—and most supportive of it—I traveled to their homelands, places that also happen to be known for striking longevity and hale residents. This journey involved studying and sampling cuisines from Greek shores to the bustling streets of Seoul, from rustic barns in the Swiss Alps to the exacting cuisine of Tokyo, to learn more about how foods might help our microbes help us. And I found many delicious meals and possibly a healthier, more diverse microbiome along the way.

So, for the benefit of our microbes and ourselves, let’s go see what millennia of human creativity and culture hath wrought. Let’s seek out some of those traditions that are feeding long-lived people and their microbiota—keeping both alive, healthy, and maybe even a little happier.

Let’s discover how to better culture ourselves.

CHAPTER ONE

•  •  •  •  •

Microbes

In Our Guts and Under Fire

The journey to a better-cultured microbiome begins with a better understanding of just what our microbiome is—and how we have been unwittingly shaping it all our lives. Let’s start this trek by taking a closer look at just how our micro-coinhabitants make their home in our bodies—and how our lifestyles have been affecting them.

Most of our microbes are concentrated in our guts.* Some of them live there full time, whereas others are just passing through. That these microbes are there at all is a recent revelation in itself. And their outsize role in our physical and psychological well-being may take yet further getting used to.

To start learning about the relationship between microbes and our health, let’s start by breaking microbes into two key human-based categories: those that live permanently in the human gut and those that don’t. This dichotomy is simplistic and not exactly how the microbes would see it, but it is a key distinction that is too often left out of conversations about our gut microbiota—especially as it relates to food. And it is one that leads to a lot of confusion about just what we should do with all of the new information we’re gleaning about our important inhabitants.

This difference is usually glossed over or omitted entirely amid the surging enthusiasm for live fermented probiotic foods, which are those that contain strains of bacteria or fungi that have been shown to have a beneficial effect on health. Instead, we get distracted by the most inventive new kombucha flavor, the best kale kimchi, or the most local goat-milk kefir. And who can blame us? These are interesting, live, effervescent cultured foods. But the microbes in our probiotic foods don’t actually take up residence in our guts. They can be valuable for health, but they are not, generally speaking, replenishing an anemic microbiome. And by focusing solely on these, we are neglecting the upkeep of our full-time microbes. In fact, what our native microbes need is fiber. Complex, rustic, now-elusive fiber. These microbe-feeding prebiotics provide the food your permanent gut residents depend on to get by.

Hi, I Live Here

The microbes that reside more permanently in our guts, day in and day out, did not come from yogurt or from kimchi. They are our native microbes. These microbes are acquired at birth, throughout infancy, and in early childhood—with a few picked up here and there later in life.

These gut microbes are essential to our health and survival. They help train our immune system. They are in constant conversation with our nervous system. And they help keep the delicate balance of our guts. These microbes evolve to their environment, says Justin Sonnenburg, a microbiologist and immunologist at Stanford University. And we may have evolved to them. He notes that we don’t just have a random collection of microbes that we pick up—we’re passing microbes to each other and through generations. Through millennia of adaptive evolution, these humble intestinal microbes have come to be some of our best allies.

Who are these unseen friends? Our guts are usually dominated by bacteria from the Bacteroidetes and Firmicutes phyla,* which together make up about 80 percent of our microbes (though there are at least ten other phyla that make appearances). Firmicutes include the familiar Lactobacillus genus.* Bacteroidetes include Bacteroides and Prevotella, among other genera. Another common phylum, especially early on in life, is Actinobacteria, in which the Bifidobacterium genus is found (which happens to be a common component of breast milk, the original probiotic).* These groups of microbes are not exclusive to the human gut. But some species of them can live only there. Our guts are their planet Earth.

Within the gut, these populations are dynamic. Most individual microbes have very short lives. So you will wake up with entirely new generations of them each morning. Some, such as members of the genus Lactobacillus, cycle through their whole lives in as little as twenty-five minutes. Others live and die even more rapidly. So while you were dreaming about that corn dog last night, your gut populations of lactobacilli could already be twenty generations beyond those you fell asleep with. That’s the relative time scale between you and your ancestors who lived in the 1500s.* And a lot of changes can happen in those generations of microbes. Especially if something in their environment shifts, such as an increase in pH (a drop in acidity), an introduction of a new food, a lack of the microbes’ preferred fiber, or an atomic bomb of antibiotics.

Hello, We’re Just Passing Through

Generally speaking, the gut isn’t a naturally friendly place for microbes. Our digestive tract is a hostile environment by design. An acidic stomach helps break down food for easier digestion, but it also disarms many of the foreign organisms—from viruses to bacteria—that we come across every day. Additionally, the gut is ideally a crowded microbial metropolis, and most outsiders just can’t cut it. As fermentation guru Sandor Katz puts it, the intestine is a competitive environment. The bacteria that are there don’t just move over and say, ‘Oh, yeah! Come on! Welcome, neighbor!’ It’s a microbe-eat-microbe world in there. All of this is a good thing for us. Only rarely does a microbe—harmful or otherwise—actually manage to endure digestion and multiply in our system.

There are, however, some microbes that can survive the harsh journey. A handful of these cause illness, such as certain strains of Escherichia coli. Most are probably nominally neutral. And a small fraction are actually beneficial.

Good, bad, or innocuous, though, none of these microbes are truly in our guts to stay.

I do hate to burst your highly cultured bubble. But with a spoonful—or crate-full—of yogurt, you have not actually reestablished your native gut bacteria, restoring you to peak ancestral intestinal health. No matter what the marketing will have you believe, and no matter how many live and active bacteria or strains are included. These microbes are perfectly happy biding their time in an aqueous world of lactose-filled yogurt. And they can, astoundingly, persevere through the acid-filled digestion process. But they are just not as well suited to long-term life in the human intestine.

But why not? In our attempt to supplement our diet with beneficial microbes, are we selecting the wrong ones? Even with all of our sophisticated screening techniques, are we being too narrow-minded in picking probiotic microbes? Are our busy native microbes to blame for crowding out these potentially beneficial bugs? Surely with a little more science, we can recalibrate our functional foods to contain microbes that could make the cut permanently in our guts, right?

One group of scientists undertook a clever study to find out why probiotic microbes weren’t taking up residence in the gut. They started with so-called germ-free mice (those raised in a totally sterile environment with no microbes inside or out), who would have no native microbes to outcompete new microbes. Then they collected soil from a warm, acidic, microbially rich swamp, finding this location to be environmentally similar to a mouse gut, and thus a good breeding ground for microbes that would survive and thrive in those murine intestines. However, after many attempts to populate the empty guts of the mice with this rich soup of candidates, not one of the microbes survived for the long term. Even with so many potential residents and wide-open intestinal landscapes, there weren’t any permanent takers. All of the microbes were adapted to live and thrive in a swamp, not in a mouse’s gut, despite the seemingly similar climates.

Many of our probiotic microbes—whether from yogurt or a capsule—are a bit like these swamp microbes. They can survive in the environment, but they aren’t cut out to live there long term. They’re mostly just along for the ride. Scientists have found, for example, that one to three weeks after you have consumed a probiotic, it’s hard to detect any trace of the introduced species. That might be bad news if you were hoping that the yogurt you ate last month would keep your microbiome replenished for years to come.* But as scientists point out, it’s not necessarily a negative that these food-based microbes don’t take up permanent residence in our intestinal tracts. Perhaps we don’t want them there forever. After all, evolution has had a long time to tailor our intestinal guest list to just the right mix. And we humans don’t always get it right when it comes to messing with ecosystems.

Just because these microbes are transient, though, let’s not write them off entirely. In fact, they are actually where things start to get interesting. Many of these dietary microbes get swept right through the whole system with your meals. Others might linger awhile in the small or large intestine. But while they are in our intestines, they are all still doing things. If you think of an individual ant passing through a picnic, you wouldn’t expect it to have much of an effect. But if you imagine a full colony of ants moving through day after day after day, you might expect to see some changes. You see, microbes eat, metabolize, and excrete as they go—not just when and where they’ve taken up permanent residence. So any compounds a microbe consumes or produces in your intestines can change its environment—and potentially the host.* Researchers are even beginning to suspect that a microbe’s physical presence alone (thanks to the proteins on its surface) might be enough to have an impact on our immune systems.

•  •  •  •  •

If microbes are such an important part of our health, what have we been doing to help them throughout the years? A casual survey of many of the world’s traditional diets suggests that over time, groups of people—cultures*—have adapted their diets to nourish and protect themselves by also nourishing and protecting their microbiota. When New York chef David Chang, creator of the Momofuku restaurants, speaks about creating foods with microbes, he uses words like indigenous, native, and even stewardship. These terms could come from a discussion of anything from flora to anthropological literature. Our overlooked microbial landscape and cultures deserve this kind of vocabulary as well. In fact, as we will see, they are deeply intertwined with our own places and human cultures.

After thousands of years of eating traditionally, eating culturally, science started to get in the way. In the nineteenth century, Louis Pasteur popularized the notion of germ theory, asserting that microbes (not miasmas*) transmit disease. Since then, we have been diligently expunging microbes from our foods and our environments.* And even though food-based probiotic microbes might not be as stalwart as we had once supposed, their presence in our diets can still be consequential—provided we consume them frequently.

Our Starving Microbes

Just as we began pasteurizing with abandon, we were also ramping up other aspects of the industrial food machine. The twin blows of refining fibers out of foods and introducing a vast array of simple carbohydrates began depriving our resident microbes of their preferred food.

Without giving a hoot about these local beneficial microbes, we’ve pushed away thousands of years of evolved, traditional diets and placed sliced bread—or more recently, perhaps, fortified snack bars—on the ultimate pedestal. We have forgone the balance of ancestral cuisines in favor of flavor and marketing. We have cast aside millennia of slow dietary changes, instead embracing a food culture that is built to gratify our every fleeting whim. And science has been complicit, refining and concocting ingredients at record speeds to satisfy cravings. Compare our food options to those just a few generations ago—not to mention a thousand years ago. And perhaps you can see how some things might have gotten off-kilter in our insides.

Efficient milling, mechanized just a couple of hundred years ago, enabled the easy separation of rougher elements in grains, decreasing the fiber content of common foods, such as bread and rice. Before its advent, most human diets were exceedingly rich in fiber and other nondigestible complex carbohydrates. These compounds are plentiful in many plants—including grains, as well as in seeds, legumes, and fruits and vegetables and feed the multitudes of beneficial bacteria living in our guts.

•  •  •  •  •

Most microbes inhabit a world where the main currency is the foodstuff our bodies are about to cast off. Their home is the last stop before our meals make their final exit. So, knowing what the large intestine holds, it might be a surprise to learn that the wall of this essential organ is only a single human cell thick. This thin boundary is important for nutrient and water absorption from the gut, as well as for close immune monitoring. But the integrity of the barrier (between the rest of our bodies and a tube filled with proto-feces and microbes) is obviously rather important as well. So the body has also evolved a protective mucus layer on the inside of the intestinal wall to help put some extra distance