Table Of ContentM. Andrea Azcarate-Peril
Roland R. Arnold
José M. Bruno-Bárcena Editors
How Fermented
Foods Feed a
Healthy Gut
Microbiota
A Nutrition Continuum
How Fermented Foods Feed a Healthy Gut
Microbiota
M. Andrea Azcarate-Peril • Roland R. Arnold
José M. Bruno-Bárcena
Editors
How Fermented Foods Feed
a Healthy Gut Microbiota
A Nutrition Continuum
Editors
M. Andrea Azcarate-Peril Roland R. Arnold
School of Medicine School of Dentistry
University of North Carolina at Chapel Hill University of North Carolina at Chapel Hill
Chapel Hill, NC, USA Chapel Hill, NC, USA
José M. Bruno-Bárcena
Department of Plant and Microbial Biology
North Carolina State University
Raleigh, NC, USA
ISBN 978-3-030-28736-8 ISBN 978-3-030-28737-5 (eBook)
https://doi.org/10.1007/978-3-030-28737-5
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Preface
Extensive research in recent decades has helped decode the impact of diet on the gut
microbiome, together with the microbial responses to nutritional components in our
diet, which converge in a delicate and balanced choreography (when healthy) or
disarray (when unbalanced or unhealthy). With over 20 years of research expertise
in fermented food, probiotics, and the microbiome, we felt like the pieces of the
nutritional- microbial puzzle had started to fit together: could it be possible that our
gut microbiota needs “reseeding” and that reseeding is done by the foods we eat?
Can food have a restorative role as a microbe provider for the gut microbiota?
Traditionally, fermented foods have been consumed by humans for millennia.
This method of food preservation was discovered most probably by accident as a
means to prevent spoilage and, unsuspectingly to the consumer, provided our ances-
tors with beneficial bacteria that repopulated the gut microbiota upon consumption.
However, novel methods of production and conservation of food have severed the
ties between the food we consume and the gut microbiota. As a consequence, there
is a documented increase in the prevalence of autoimmune diseases and obesity,
which has been correlated to a decreased diversity of gut microbes, while infectious
disorders have decreased in the past decades.
This book offers an introduction dedicated to the environmental microbiome as
the piece that completes the circle of life or the “nutrition continuum.” After the
introduction, we have structured the book in three parts. The first one focuses on
food and its associated microbes. From breast milk to fermented food, it is clear
that food is responsible not only for providing nutrition to the host but also for
“seeding” the gut-associated microbiota. The chapters in this part provide an over-
view of what is currently known about the microbes associated with breast milk
and fermented food and recount traditional forms of food preparation with current
industrial techniques in terms of the potential loss of microbial diversity associated
with industrialization.
We dedicated the second part of this book to the mouth and its associated
microbes. The mouth environment and the oral microbiota are clearly the gatekeep-
ers and main microbial contributors to the gut microbiota through food and shed-
ding of microbes. Moreover, the lack of a clear demarcation between the external
v
vi Preface
environment and the oral cavity has resulted in a unique environment, which hosts
a complex and diverse microbiota. In addition, the technical accessibility of the oral
microbiota to sampling has allowed significant advances in microbiome research
that reveal clear relationships between oral and gut health.
The final segment of our book looks into the gut microbiota across ages, starting
with the lifelong consequences of the infant’s initial colonization period, following
with chapters on the gut microbiota during adulthood and aging. The next chapters
attempt to answer questions regarding how we can beneficially modulate the micro-
biome with probiotics and prebiotics to rebalance a gut microbiota skewed by the
modern practices of our Western society.
We are extremely grateful to the contributors of this book. Their outstanding
intellectual contributions and scientific expertise made this project possible. We are
also thankful to our colleagues, Apoena Ribeiro, Jason Arnold, Sue Dagher, and
Hunter Whittington, for their critical reading of all or parts of the manuscript.
We live in a time where relevant scientific questions can be readily answered,
thanks to available technologies. However, too often, discoveries and rational scien-
tific conclusions are not translated into policies that benefit humankind but instead
relegated by political and economic decisions with costly consequences. We hope
that this book conveys the importance of making good personal and collective deci-
sions in terms of nutritional behaviors that greatly affect human health.
Chapel Hill, NC, USA M. Andrea Azcarate-Peril
Chapel Hill, NC, USA Roland R. Arnold
Raleigh, NC, USA José M. Bruno-Bárcena
Introduction: The Ancient Symbioses
I started off my career focused on social insects and the species that live with them.
At the age of 19, I worked with James Danoff-Burg, then a graduate student at the
University of Kansas, to study a group of beetles that live inside the colonies of
Linepithema ants in the deserts of the southwest. Then the next year, I accepted a job
working with Samantha Messier, then a graduate student at the University of
Colorado, Boulder. Sam was studying a species of termite common in the forests of
the Neotropics, Nasutitermes corniger. These termites are amazing for a variety of
reasons, but one of them is the fact that the soldiers of Nasutitermes corniger have,
in place of ordinary insect weaponry (spines, spines, stings, or mandibles), long
noses. Out of these noses (nasutes), the soldiers shoot a mix of terpenes that is
gooey and smells a bit like turpentine. This mix helps to defend the termites against
ants and also anteaters. To me, as a then 19-year-old, that such elaborate chemical
weaponry was to be found amid nonhuman societies was mind blowing. But spray-
ing turpentine is not the best trick of which Nasutitermes termites are capable,
not hardly.
The Nasutitermes soldiers, although endowed with great biochemical power,
also have a weakness. They lack functional, chewing mouthparts. They cannot eat
on their own and so rely on their brothers and sisters to feed them. But even after
being fed by their brothers and sisters, the soldiers are still wanting in some nutri-
ents, particularly nitrogen. The soldiers cope with this problem by playing host to
bacteria that fix nitrogen from the air—“From the air!” This was really too much for
me to believe, a bit of nature inspired by magical realism, and yet it was true.1
What I would go on to study with Sam was whether the termite soldiers (and
workers) rely more on their nitrogen fixing microbes when the wood they eat is low
in nitrogen and when they are actively at war with anteaters. Here then was my
actual job—I was to be the anteater. My role for three months at the La Selva
Biological Station in Costa Rica was to attack the colonies of this very sophisticated
1 Prestwich, Glenn D., and Barbara L. Bentley. “Nitrogen fixation by intact colonies of the termite
Nasutitermes corniger.” Oecologia 49, no. 2 (1981): 249–251.
vii
viii Introduction: The Ancient Symbioses
termite with a very unsophisticated machete and see if, once attacked, they would
produce more soldiers (they did), which, in turn, would fix more nitrogen (they did),
thanks to their gut microbes.2
At that time, the idea that termites rely on gut microbes was not novel. The very
first study of the role of gut microbes in nutrition was that of Joseph Leidy on the
guts of termites, which was published in 1881.3 In the years since, it had been estab-
lished that the guts of termites are full of many kinds of microbes, be they bacteria,
protists, symbioses between bacteria and protists or even archaea. These relation-
ships are, it had been shown by then, relatively fine-tuned to the life history of the
termites. Grass-feeding termite species have different gut microbes from wood-
feeding termite species, which, in turn, have different microbes from soil-feeding
termite species.4 The bodies of termites have slightly diversified over the last hun-
dred and fifty million years, but their guts and the microbes in them have diversified
greatly, including, in the case of Nasutitermes, the origin, evolution, and elaboration
of relationships with nitrogen-fixing bacteria.
As a 19-year-old, it seemed obvious to me that if termites hosted microbes on
which they depended, then other insects in the forests around me probably did as well
(why wouldn’t they?) It also seemed reasonable to me, and I suspect to anyone study-
ing termites and their microbes, that so too did the birds and mammals I was not
alone. Amid beer drinking and banjo playing at the research station where I studied
termites, scientists speculated about whether the world was, if viewed through a
microbial lens, one in which microbes carried out basically every process and some-
times, when they needed to, made animals carry them from place to place or, figura-
tively speaking, hold their sandwich.5 But none of these ideas, although in many
ways obvious, were terribly mainstream. Microbial symbioses were being studied by
insect biologists or animal scientists in agricultural colleges and land grant institu-
tions (like the one in which I now work).6 Such studies, we know in retrospect, would
prove central to understanding the biological world. But they were not central to the
fields of ecology and evolutionary biology. Nor were they especially central to the
story of human health. Theses, great thick theses, need to be written about why sym-
bioses between microbes and their hosts, and the study of those symbioses, stayed in
the margins for so long. Regardless of its cause the marginal status of the study of
symbioses would eventually change. The role of microbes associated with animals
2 Messier, Samantha Hope. “Ecology and division of labor in Nasutitermes corniger: The effect of
environmental variation on caste ratios.” (1997): 2298–2298.
3 Leidy, Joseph. Parasites of the termites. Collins, Printer, 1881.
4 Ohkuma, Moriya, and Andreas Brune. “Diversity, structure, and evolution of the termite gut
microbial community.” In Biology of termites: a modern synthesis, pp. 413–438. Springer,
Dordrecht, 2010.
5 Dyer, Betsey Dexter. “Symbiosis and organismal boundaries.” American Zoologist 29, no. 3
(1989): 1085–1093.
6 RE Hungate’s important work spanned both of these fields. He began with termites and moved on
to ruminants. Hungate, R. E. “The symbiotic utilization of cellulose.” Journal of the Elisha
Mitchell Scientific Society 62, no. 1 (1946): 9–24.
Introduction: The Ancient Symbioses ix
and plants would rise in prominence. This rise began in part due to the arrival of novel
approaches to the study and the identification of microbes and sequencing-based
approaches.
The availability of novel sequencing approaches (approaches made possible by
using enzymes from microbes themselves, like those of Thermus aquaticus) changed
everything. With new barcoding and metagenomics tools, it became possible to
relatively quickly do an inventory of the kinds of life in a given place. In some sub-
fields, these new approaches could be combined with insights from earlier work on
insects or domestic animals to jump-start discoveries. In other cases, the new wave
of research began as if from scratch (even where antecedents). As tens and then
hundreds and then thousands of studies accumulated, it became ever clearer that
humans are covered with microbes, that humans are filled with microbes, and that
human food too, much of it anyway, is rich with microbes. Of course, these insights
were not really new. They were instead newly appreciated and, thanks to the new
sequencing approaches (and the new waves of funding that they would usher in),
were no longer marginal. The microbe was out of the bag (or out of the gut, as the
case might be). Humans are, just like all the species, filled with species on which we
depend. We are like the termites, just bigger and gassier. The study of insects, agri-
culture, ecology, evolution, and medicine began to acquire a new holism, a holism
made possible by the ubiquitous importance of microbes.
But there was a problem. In the years between the first studies of the gut microbes
in termites and the re-recognition of the value of the microbes on and in our bodies
and in our food, we had, collectively as humans, made a mistake—a very big mis-
take, a no good, stinking, terrible mistake. The mistake we made was simplifying
the microbial communities present in our lives, dramatically. We overused antibiot-
ics for diseases that were not bacterial. We used antimicrobials in settings where
soap would have been used. We closed our windows and sealed out plant- and soil-
associated microbes. We also increasingly shifted to processed food, in which wild
microbes were rare, as were those associated with fermentation, and in their place
were an abundance of microbes adapted to do well in freezers and refrigerators. To
use the language of ecologists, these changes changed our Western baseline, they
changed the condition of the body and daily life of the average person, they changed
it so much that it sometimes made it difficult for us to tell exactly what is wrong.
Rare chronic diseases, diseases related in one way or another to changes in the
microbes in our lives, became common. Crohn’s disease, inflammatory bowel dis-
ease, multiple sclerosis, allergies, asthma, and maybe even autism all fall within this
circus of terrible modern maladies.
Some features of the future of the study of our bodies, our microbes, and our new
chronic maladies seem predictable. It seems predictable, for instance, that the
microbes we need in our environment, on our food, and in and on our bodies will be
shown to depend both on our genes and on our lifestyles. It seems predictable that
there will not be one kind of “healthy microbiome” but many instead. This, after all,
is what was found with the termites. When the termites had less access to wood with
lots of nitrogen, they needed (and typically hosted) more nitrogen-fixing bacteria.
When they went to war, whether against real anteaters or against my machete, they
x Introduction: The Ancient Symbioses
needed more nitrogen-fixing bacteria. We should not expect our own bodies to be
any simpler, and, indeed, given the great diversity of human genetic backgrounds
and experiences, we are likely to be much, much more complex.
This book attempts, in light of our broad human story, and in light of a particular
moment in the history of science, to consider what we know right now about
microbes, health, and nutrition. It considers the microbes of the mouth, microbes in
food, gut microbes, and our wellness. The authors in this book do not all agree with
each other about just which set of microbes benefit us and when. They do not all
agree with each other about many features of our bodies, microbes, and wellness—
as it should be. We do not yet understand enough about ourselves to understand the
simple answers, and so instead what we have begun to develop are kinds of regulari-
ties, things that seem to be mostly, but not always, true. Fermented food, when still
alive, seems to offer health benefits—often but not always. The Western diet, rich in
sugar, seems to lead to microbes in mouths that are less healthy and more likely to
cause cavities—often but maybe not always.
The book is, as far as I know, the first of its kind, the first to think about what it
would look like to eat food that benefits us and our beneficial microbes. Or rather, it
is the first of its kind for humans. In this way, one of the most beautiful things about
what this book offers is that it draws humans back into the rest of life. It reminds us
that we are not only connected to and dependent upon the microbes that we ingest
or fail to ingest and rub upon but also that this condition unites us with every other
species of animal that has ever lived. We humans are special in our consciousness,
in our ability to think about problems, and we actively make decisions about the
change we would like to make. But in a microbial context, we are also unusual in
that we need this book. For three hundred million years, animals acquired the
microbes they needed without problem, from their food and their environments,
without need to figure out how to do so. We are uniquely the species that has altered
our environment and our diet so completely that we need to study how to do what
other species do without thinking. This book then is the beginning of the grounding
we need in order to remember how to be like the other species and remember, in
other words, how to be microbially whole.
Natural History Museum of Denmark Rob R. Dunn
Copenhagen, Denmark
Department of Applied Ecology
North Carolina State University
Raleigh, NC, USA
