Tuesday, October 22, 2013

Gut Microbes May Drive Evolution - Micro-organisms, the Microbiome, and the Holobiome


Over the last decade or so, biologists have identified and mapped nearly all of the micro-organisms that together comprise the microbiome, and in doing so they have also developed an ever-growing appreciation for the essential role of our microbial communities in health both mental and physical. The DNA of these micobiota outnumbers human DNA by 10 to 1, weight somewhere between 7 oz. an 48 oz.
A microbiome is "the ecological community of commensal, symbiotic, and pathogenic microorganisms that literally share our body space."[1][2] This term was originally coined by Joshua Lederberg, who argued the importance of microorganisms inhabiting the human body in health and disease. Many scientific articles distinguish "microbiome" and "microbiota" to describe either the collective genomes of the microorganisms that reside in an environmental niche or the microorganisms themselves, respectively.

Further, there is a related model of evolution based on the impact of the microbiome on our own genetic and epigenetic evolution, the hologenome theory of evolution. The hologenome theory of evolution proposes that the object of natural selection is not the individual organism, but the organism together with its associated microbial communities.

In this model, although not universally, microbiota are re-termed symbionts, while the hologenome is re-termed the holobiont, a term that represents the symbiotic relationship between the host and its symbionts.
[R]elationships (ranging from mutualism to parasitism) lead to formation of a holobiont [1,2] that includes host and its associated microbiota or symbionts (Figure 1). Although the word “Holobiont” was coined by Lynn Margulis in 1991, to signify symbiosis between individual organisms or the bionts [1], the concept was highlighted in 2002 and later during the study of corals, and their associated symbionts, as coral holobionts [2].
This is not a new idea in evolutionary theory, but until 15-25 years ago, we did not understand how it worked so mainstream evolutionary biologists dismissed it. Now it is known, sometimes derisively, as Neo-Lamarckism within a Darwinian context.

The microbiome has become a popular topic in the media. A recent CBS News article proclaimed "How the gut's "microbiome" affects weight gain," the Digital Journal reported on the "Immune system and skin microbiome," Gastroenterology and Endoscopy News claim that "Ideas About Gut Microbiome and Diet Becoming Mainstream," while a recent Huffington Post Canada, "Thinking of Going Gluten-Free? Why Your Gut Will Thank You,"argued that going gluten free will change the balance of microbiota from pro-inflammatory to anti-inflammatory.


According to William Davis (in the Huff Post article):

"We've had decades of research on wheat and gluten's effects on the body and we know the microbiome is involved. Although we may not know all of the links at the cellular and molecular level, we can still improve our lives now. By avoiding wheat, people can keep their germs happy, their immune systems balanced and improve the quality of their lives. I think it's worth the effort."
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Before launching into this too brief article, here are a couple of definitions from Wikipedia (microbiome) and the journal Gut Pathogens (hologenome):

Microbiome

File:Skin Microbiome20169-300.jpg
  Depiction of the human body and bacteria that predominate

A microbiome is "the ecological community of commensal, symbiotic, and pathogenic microorganisms that literally share our body space."[1][2] This term was originally coined by Joshua Lederberg, who argued the importance of microorganisms inhabiting the human body in health and disease. Many scientific articles distinguish "microbiome" and "microbiota" to describe either the collective genomes of the microorganisms that reside in an environmental niche or the microorganisms themselves, respectively.[3][4][5] However by the original definitions these terms are largely synonymous.

The human body contains over 10 times more microbial cells than human cells, although the entire microbiome only weighs about 200 grams (7.1 oz),[6][7] with some weight estimates ranging as high as 3 pounds (approximately 48 ounces or 1,400 grams). Some consider it to be a "newly discovered organ" since its existence was not generally recognized until the late 1990s and it is understood to potentially have overwhelming impact on human health. Modern DNA testing of their residues has enabled researchers to find the majority of these microbes, since the majority of them cannot be cultured in a lab using current techniques. Its most important aspect may be its possible effect on auto-immune diseases like diabetes, rheumatoid arthritis, muscular dystrophy, multiple sclerosis, fibromyalgia, and perhaps some cancers. Common obesity might also be aggravated by a poor mix of microbes in the gut. Since some of the microbes in our body can modify the production of neurotransmitters known to be found in the brain, we may also find some relief for schizophrenia, depression, bipolar disorder and other neuro-chemical imbalances.

Microbiomes are being characterized in many other environments as well, including soil, seawater and freshwater systems. It is believed that Endosymbiotic theory originally gave rise to more complex organisms, and continued to play a fundamental role in guiding their evolution and expansion into new niches.

The microbes being discussed are generally non-pathogenic (do not cause disease unless they grow abnormally); they exist in harmony and symbiotically with their hosts.[8]

Researchers have learned that much of the population of microbes found in the human body are not bacteria but a very old class of single-celled organisms called archaea.[8]
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The Holobiont and the Hologenome


During the course of evolution, multicellular living forms emerged from unicellular life; the latter not only predominates the multicellular life quantitatively but also has a close association with it. There are many types of associations that have developed during evolution ranging from mutualism to parasitism. Such associations always affect the life of multicellular hosts in the short term from birth to death, with implications on their survival in the environment, and in the long term as a phenotypic unit for natural selection. Such relationships lead to formation of a holobiont [1,2] that includes host and its associated microbiota or symbionts (Figure 1). Although the word “Holobiont” was coined by Lynn Margulis in 1991, to signify symbiosis between individual organisms or the bionts [1], the concept was highlighted in 2002 and later during the study of corals, and their associated symbionts, as coral holobionts [2]. Symbionts can be divided into two categories, endosymbionts and exosymbionts which refer to symbionts living inside or outside of the host cells, respectively. Such associations result in a hologenome comprising of genetic information of both host and the associated microbiota [3]. Hologenome includes the static genome of the host alongwith dynamic genome of the symbiota. The dynamism of symbiota’s genome provides the competence to holobiont to adapt and survive in different environmental conditions. The hologenome theory of evolution considers the alliance of holobiont with its hologenome as a selection unit for evolution to act upon [3]. Further hologenome theory of evolution can be helpful in comprehending the emerging constructive role of probiotics in human health.
Alrighty then . . . it seems the preface material greatly out-weighs the actual article from Scientific America, but hopefully it was interesting and/or useful.

Gut Microbes May Drive Evolution

The bacteria that live quietly in our bodies may have a hand in shaping evolution


By Carrie Arnold


WE ARE ONE: Biologists say common gut microbes such as Bacteroides fragilis may be as important as our genes. Image: Photo Researchers, Inc.

The human body harbors at least 10 times more bacterial cells than human cells. Collectively known as the microbiome, this community may play a role in regulating one's risk of obesity, asthma and allergies. Now some researchers are wondering if the microbiome may have a part in an even more crucial process: mate selection and, ultimately, evolution.

The best evidence that the microbiome may play this critical role comes from studies of insects. A 2010 experiment led by Eugene Rosenberg of Tel Aviv University found that raising Drosophila pseudoobscura fruit flies on different diets altered their mate selection: the flies would mate only with other flies on the same diet. A dose of antibiotics abolished these preferences—the flies went back to mating without regard to diet—suggesting that it was changes in gut microbes brought about by diet, and not diet alone, that drove the change.

To determine whether gut microbes could affect an organism's longevity and its ability to reproduce, Vanderbilt University geneticist Seth Bordenstein and his colleagues dosed the termites Zootermopsis angusticollis and Reticulitermes flavipes with the antibiotic rifampicin. The study, published in July 2011 in Applied and Environmental Microbiology, found that antibiotic-treated termites showed a reduced diversity in their gut bacteria after treatment and also produced significantly fewer eggs. Bordenstein argues that the reduction of certain beneficial microbes, some of which aid in digestion and in the absorption of nutrients, left the termites malnourished and less able to produce eggs.

These studies are part of a growing consensus among evolutionary biologists that one can no longer separate an organism's genes from those of its symbiotic bacteria. They are all part of a single "hologenome."

"There's been a long history of separating microbiology from botany and zoology, but all animals and plants have millions or billions of microorganisms associated with them," Rosenberg says. "You have to look at the hologenome to understand an animal or plant." In other words, the forces of natural selection place pressure on a plant or animal and its full array of microbes. Lending support to that idea, Bordenstein showed the closer the evolutionary distance among certain species of wasps, the greater the similarities in their microflora.

Researchers believe that the microbiome is essential to human evolution as well. "Given the importance of the microbiome in human adaptations such as digestion, smell and the immune system, it would appear very likely that the human microbiome has had an effect on speciation," Bordenstein says. "Arguably, the microbiota are as important as genes."

~ This article was published in print as "Backseat Drivers."
Here is a little bit on the the hologenome theory of evolution, from a 2011 article (Symbiosis and Development: The Hologenome Concept) by Eugene Rosenberg and Ilana Zilber-Rosenberg in Birth Defects Research [(Part C) 93:56–66 (2011). DOI: 10.1002/bdrc.20196].

THE HOLOGENOME CONCEPT 
The hologenome theory of evolution considers the holobiont with its hologenome, acting in consortium, as a unit of selection in evolution (Rosenberg et al., 2007; Zilber-Rosenberg and Rosenberg, 2008; Sharon et al., 2010). The holobiont has been defined as the host organism and all of its symbiotic microbiota (Rohwer et al., 2002). The hologenome is the sum of the genetic information of the host and its microbiota. The hologenome theory posits that (1) all animals and plants harbor abundant and diverse microorganisms acquiring from their host a sheltered and nutrient-rich environment, (2) these microbial symbionts affect the fitness of the holobiont and in turn are affected by it, (3) variation in the hologenome can be brought about by changes in either the host genome or the microbial population genomes (microbiome), and (4) these variations, including those of the microbiome, can be transmitted from one generation to the next with fidelity and thus may also influence evolution of the holobiont.
Fitness in the case of a holobiont must include beneficial interactions between the host and its symbionts, including those that may influence development, reproduction, and adaptation. In addition, it has to include beneficial interactions between the symbionts themselves as well as between the holobiont and other holobionts and the environment.

Variation in a holobiont can arise from changes in either the host or the symbiotic microbiome. Genetic variation in the host (occurring in the gametes or during development) as well as in individual microorganisms can be generated by the well-recognized mechanisms of recombination, chromosome rearrangement, and mutation, in addition to epigenetic variation. Stochastically produced variants followed by selection of the fittest are the essence of neo-Darwinian evolution. Consideration of the hologenome, namely the host genome combined with that of its microbiota, brings forth three additional modes of variation, which are unique to the holobiont. The first is microbial amplification, the increase of one group of symbionts relative to others, which can occur when conditions change. The holobiont is a dynamic entity with certain microorganisms multiplying and others decreasing in number as a function of local conditions within the holobiont. An increase in the number of a particular microbe is actually equivalent to gene amplification. Considering the large amount of genetic information encoded in the diverse microbial population of holobionts, microbial amplification can be a powerful mechanism for affecting adaptation and development. Examples of environmental factors that can lead to changes in symbiont populations and thereby to variation in hologenomes are nutrient availability, disease, light intensity, pH, and temperature. The second mechanism for introducing variation into holobionts is acquisition of new symbionts from the environment. All animals and plants come into contact with billions of microorganisms during their lifetime. One can reasonably assume that occasionally, as a random event, some of these microbes will find a niche and become established in the host. Under the appropriate conditions, the novel symbionts may become more abundant and affect the phenotype of the holobiont. Unlike microbial amplification, acquiring new symbionts can introduce entirely new genes into the holobiont. The third mechanism is horizontal transfer of genes from transient or nonassociated bacteria to resident microbiota.


The applied fields of prebiotics and probiotics involve attempts to modify microbiota of animals, including man, and plants, by changing the diet or adding specific bacteria, respectively. In effect prebiotics targets variation by amplification and probiotics can lead both to amplification and acquisition of novel bacteria.
Microbial amplification and acquisition of novel microbes into holobionts closely fit the Lamarckian first principle of ‘‘use and disuse.’’ The holobiont loses characteristics (microbes) it does not use and gains characteristics (microbes) that are useful. As these amplified or acquired microbes can be transmitted to offspring, it satisfies the second principle of Lamarckism. Thus, the hologenome theory of evolution contains Lamarckian principles within a Darwinian framework (Rosenberg et al., 2009). In addition, it should be pointed out that microbial variation in a holobiont can be considered an epigenetic variation, in that it involves inherited changes in the phenotype caused by mechanisms other than changes in the underlying host DNA sequence (Gilbert et al., 2010).

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