The Human Microbiome as Road Kill in the Age of the Anthropocene
With the world entering a new geological epoch – the Anthropocene – the idea that we now live in a very different world than the one our not-so-distant ancestors inhabited, has never been truer. But amidst global deforestation, melting ice sheets, and general biosphere degradation, perhaps the human microbiome – the collection of our microbiota and their genes – was an early, yet unrecognized, casualty. As a microbial canary in the coalmine, the modern human microbiome starts looking like a cog in the wheel of current ecological disasters when considered against the backdrop of our recent work among East African hunter-gatherers.
In the faint glow of the firelight, I watch as a Hadza hunter skillfully butchers a baboon and shares meat with others around the fire. Nothing goes to waste as organ meats, including the brain, are consumed along with raw colon and stomach that are eaten sushi style. By sterile western standards it’s a gruesome sight for an evening meal. No matter how many times I’ve watched Hadza carve up a myriad of animals dispatched with bow and arrow, I am still taken back by the extraordinary exchange of microbes between the Hadza and their environment – a microbial tango that likely characterized the entirety of human evolution.
Breathless news coverage on the connection between ones gut microbes and some ailment of the modern world is a near weekly occurrence. Though causality is illusive, research is connecting microbes to conditions as diverse as obesity, diabetes, autoimmune diseases, heart disease, IBS, chronic fatigue syndrome, autism, food allergies, neurological and psychiatric disorders and the list goes on – and will surely grow.
An emerging trend in this research is that microbial diversity is diminished during many of theses disease states and that a drop in ones diversity can often signal the onset of a disorder. The rub is, of course, did the disease cause the drop in microbial diversity or did the drop in diversity precede the disease? While these are early days and much work lays ahead, the idea that microbes and the diversity of microbes we carry may help us better understand and head-off disease in the twenty-first century has spawned a level of optimism in medical research not seen since the humanity-altering introduction of antibiotics over 50 years ago. Seems everyone from the White House to Wall Street is paying attention.
Which brings me back to the Hadza.
Living and working amongst the Hadza for years has brought front and center the intimate relationship humans have likely evolved with diverse groups of microbes. With each animal killed, microbes are given the opportunity to move from one species to the next – so long as they can find a suitable niche. With each berry that is plucked from a bush or tuber dug from beneath the microbial-rich ground, each and every act of foraging keeps the Hadza connected to an extensive regional (microbial) species pool.
From high in the mighty baobab tree, where Hadza climb to gather natures most energy dense food – provided by African honey bees – to the pools of drinking water dotting the landscape to the feathers from a bird felled by a Hadza arrow, each touch point on the landscape is linked in a microbial network that runs through the gut of every Hadza.
My colleagues and I have collected thousands of stool, skin, oral and environmental samples of all kinds, ranging from water sources throughout Hadza land, to swabs of grass huts, tubers, berries, food preparation areas and so on. Because the Hadza dispatch a wide range of wild animals, including a dizzying diversity of birds, we’ve amassed an impressive microbial sample of African fauna. Each sample is stored in the field in liquid nitrogen and kept frozen until it reaches labs back in states. Using next generation sequencing technology, we’ve started to characterize the microbes living on and within the Hadza and across their larger regional species pool. It is their persistent exposure to this regional microbial pool that has endowed the Hadza with an extraordinary diversity of microbes – much greater than we see among populations in the so-called developed world.
Viewed through the lens of ecological theory, our less diverse gut microbiome in the west can potentially be seen as either a function of a degraded regional species pool, an increase of environmental filters that limit the immigration of microbes from the regional pool to local communities (us), or a combination of both. I would argue that much of our attention has been focused on environmental filters – or species sorting – as the primary culprit to the detriment of the equally important contribution of the regional species pool.
A classic example of an environmental filter would be the overuse of antibiotics that, with each course, reduce the diversity of microbes in the host. Other filters may include that we spend too much time indoors, increased caesarean births, reduced breast feeding rates, antimicrobial soaps, skin and hair products, sub-therapeutic levels of antibiotics in livestock, and possibly even chlorinated water and various forms of modern hygiene are all, potentially limiting (filtering) nature’s time-honored immigration. Diet, modern food production, packaging and preparation – from plough-to-plate – can and surely selects for local (us) microbial communities that are greatly depleted than less filtered communities (e.g, the Hadza).
But the contribution of regional species pool gets little attention in microbial research and almost no media attention – though it’s a central theme in ecology, though more focused on macro-organisms. Considering our classic environmental filtering example above, antibiotics, one wonders if someone who took an antibiotic and experienced a reduction in microbial diversity wouldn’t recover more quickly – that is, exhibit greater resilience – if they had a access to a robust and diverse regional species pool once the perturbation was released?
There are hints that contact and access to a diverse regional species pools is crucial. In Finland, researchers found that lack of species richness in certain plant communities around homes effected skin bacteria that in turn were strongly associated with atopy, a common immune dysfunction of the modern world. In another study, skin bacterial communities of Red-backed salamanders showed marked decrease in richness and evenness if they were deprived of their natural, microbial-rich soil reservoir compared to salamanders housed with a soil reservoir.
Currently 50% of the world’s population lives in urban areas characterized by reduced biodiversity – both at a macro- and microorganism scales. This is expected rise to 60-70% by 2050 for developed countries. Clearly today’s biosphere and the regional species pool available to colonize humans and other hosts are changing under unprecedented anthropogenic disturbances such as urbanization. No doubt a Hadza hunter-gatherer relocated to an urban city in Europe would undergo a rapid drop in microbial diversity. The question being, of course, is this a function of local environmental filters and species sorting due to things like diet and hygiene, or a degraded regional species pool that would otherwise provide new immigration to offset the extinctions created by the filters?
Someone wise once said microbiome research isn’t rocket science, it’s actually harder. Decoupling the effect of environmental filters (e.g., diet, antibiotics, built environment, hygiene, birthing method) on local microbial communities (e.g., us, our homes) from the diversity and dispersal characteristics of regional species pools is a much-needed area of research. But we also must consider the possibility that our regional species pools – once teaming with microbial life with few barriers to immigration to local communities – has undergone a dramatic change in the age of human made ecological calamity – the Anthropocene.
Surely better ecological management of environmental filters in developed countries at the personal and policy level would pay dividends in improving potentially beneficial microbial diversity at the individual, family and larger community level. However, armed with a better understanding that regional and global ecological degradation and disaster may be hitting a little closer to home than most of us previously imagined (our own gut), may provide a much-needed on-ramp that this generation needs to finally put the health of ecosystems – large and small – into perspective. Open-source efforts like American Gut and MapMyGut, which afford average citizens around the world access to their own microbial inhabitants through citizen science, represent a teaching moment to mobilize this much-needed group of micro-environmentalists.
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