Nature

Scientists Rethink the Traditional Approach to Microbes

October 30, 2015 | Sarah Tse

Woman, magnifying glass, microbes, microbiome

When John Donne proclaimed, “No man is an island entire of itself,” he probably wasn’t talking about the countless bacteria living within our bodies. But a new study suggests that these microbes shape our health, development, and interactions with the environment.

A scant 10 percent of the cells in your body are human. The other 90 percent are bacteria of all different kinds — and they’re not just passive passengers along for the ride. These bacteria play a vital role in defining who you are and how you function as a biological unit.

SEE ALSO: Forget Fingerprints. You Can be Identified by Your Microbial Cloud.

The mounting evidence for the significance of the microbiome has led two scientists to propose a fundamental shift in mindset that applies microbial knowledge to existing biological principles. Their article, published in PLOS Biology, establishes a new paradigm almost Darwinian in scope, although fortunately it has found a more receptive audience.

The authors assert that holobionts are a fundamental unit of biological organization that must replace our conception of multicellular organisms as autonomous individuals. The collective genes of the hologenome interact and behave just like genes within a single cell, with mutations as the basis for variation among those genes.

This isn’t exactly old news. Biologists have known that we are not alone in our bodies for decades now. The term “microbiome,” referring to the community of microbes that live inside our bodies, was first coined in 2001 by Josh Lederberg, and since then scientists have published study after study examining the interplay between organisms and the micro-organisms within them.

For example, evolutionary biologists believe that the symbiotic relationship between plant hosts and microscopic fungi was crucial in helping plants to colonize land 4 hundred million years ago. Bacteria living in the roots of legumes like peanuts perform nitrogen fixation, which turns inert atmospheric nitrogen into a form the plant can use as fertilizer.

In terms of animal-microbe relationships, digestion of tough plant materials would not be possible without a lush microcosm of bacteria living in the gut, particularly in ruminants like cows and goats where digestion is an epic process spanning several days. But when the gut microbes run rampant, they can also cause a variety of diseases and disorders, from type I diabetes and obesity to depression, anxiety, and autism.

So it’s clear that the influence of microbial passengers is in no way proportional to their size. Microbiologists use the term “holobiont” to describe the complex network of host plus microbes, and “hologenome” to refer to its collective genetic identity.

This new paper takes the hologenome concept further by applying it to evolution. High school biology classes have hammered home the falsity of Lamarck’s theory that organisms can pass on acquired traits to their offspring. The hologenome concept subverts this previously firm understanding of evolution: interactions with the environment during the host’s lifetime can actually alter the diversity of the microbiome and the genes it contains, and these changes can then be inherited by the host’s offspring.

This new concept must also change how we think about the mechanism of natural selection. We already know that species with intimate ecological relationships, like predators and prey or a pollinator and flower, exert selective pressures on each other and co-evolve. Considering each of those players as holobionts makes the picture far more complicated. Indeed, variations in the microbiome can even drive the creation of new species amongst the hosts: a previous study by one author demonstrated that two wasps with sufficiently different microbial populations were unable to successfully reproduce.

This new framework demands that researchers take a more holistic approach, or risk producing useless or even misleading data. Ever since we first discovered microbes, we have feared them as disease-causing invaders of the sanctity of our bodies. But ignoring their crucial impact on the structure of the living world will only hamper any efforts to advance science.

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