Dead guts spill history of extinct microbes: Fecal samples from archeological sites reveal evolution of human gut microbes

Dec. 12, 2012 — Extinct microbes in fecal samples from archaeological sites across the world resemble those found in present-day rural African communities more than they resemble the microbes found in the gut of cosmopolitan US adults, according to research published December 12 in the open access journal PLOS ONE by Cecil Lewis and colleagues from the University of Oklahoma.

The researchers analyzed 1400-8000-year-old fecal samples preserved at three archaeological sites: natural mummies from Caserones in northern Chile, and samples from Hinds Cave in the southern US and Rio Zape in northern Mexico. They also used samples from Otzi the Iceman and a soldier frozen on a glacier for nearly a century. They compared the now-extinct microbes in these samples to microbes present in current-day soil and compost, as well as the microbes present in mouths, gut and skin of people in rural African communities and cosmopolitan US adults.

The authors discovered that the extinct human microbes from natural mummies closely resembled compost samples, while one sample from Mexico was found to match that from a rural African child. Overall, the extinct microbial communities were more similar to those from present rural populations than those from cosmopolitan ones. The study concludes, "These results suggest that the modern cosmopolitan lifestyle resulted in a dramatic change to the human gut microbiome."

As Lewis explains, "It is becoming accepted that modern aseptic and antibiotic practices, are often beneficial but come with a price, such as compromising the natural development of our immune system through changing the relationship we had with microbes ancestrally. What is unclear is what that ancestral state looked like. This paper demonstrates that we can use ancient human biological samples to learn about these ancestral relationships, despite the challenges of subsequent events like degradation and contamination."

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Raul Y. Tito, Dan Knights, Jessica Metcalf, Alexandra J. Obregon-Tito, Lauren Cleeland, Fares Najar, Bruce Roe, Karl Reinhard, Kristin Sobolik, Samuel Belknap, Morris Foster, Paul Spicer, Rob Knight, Cecil M. Lewis. Insights from Characterizing Extinct Human Gut Microbiomes. PLoS ONE, 2012; 7 (12): e51146 DOI: 10.1371/journal.pone.0051146

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How common 'cat parasite' gets into human brain and influences human behavior

Dec. 6, 2012 — Toxoplasma is a common 'cat parasite', and has previously been in the spotlight owing to its observed effect on risk-taking and other human behaviours. To some extent, it has also been associated with mental illness. A study led by researchers from Karolinska Institutet in Sweden now demonstrates for the first time how the parasite enters the brain to influence its host.

"We believe that this knowledge may be important for the further understanding of complex interactions in some major public health issues, that modern science still hasn't been able to explain fully," says Antonio Barragan, researcher at the Center for Infectious Medicine at Karolinska Institutet and the Swedish Institute for Communicable Disease Control. "At the same time, it's important to emphasize that humans have lived with this parasite for many millennia, so today's carriers of Toxoplasma need not be particularly worried."

The current study, which is published in the scientific journal PLoS Pathogens, was led by Dr Barragan and conducted together with researchers at Uppsala University.

Toxoplasmosis is caused by the extremely common Toxoplasma gondii parasite. Between 30 and 50 per cent of the global population is thought to be infected, and an estimated twenty per cent or so of people in Sweden. The infection is also found in animals, especially domestic cats. People contract the parasite mostly by eating the poorly cooked flesh of infected animals or through contact with cat faeces. The infection causes mild flu-like symptoms in adults and otherwise healthy people before entering a chronic and dormant phase, which has previously been regarded as symptom-free. It is, however, known that toxoplasmosis in the brain can be fatal in people with depleted immune defence and in fetuses, which can be infected through the mother. Because of this risk, pregnant women are recommended to avoid contact with cat litter trays.

A number of studies have been presented in recent years showing that the toxoplasmosis parasite affects its host even during the dormant phase. It has, for example, already been observed that rats become unafraid of cats and even attracted by their scent, which makes them easy prey. This has been interpreted as the parasite assuring its survival and propagation, since the consumed rat then infects the cat, which through its faces can infect the food that other rats might then proceed to eat. A number of studies also confirm that mental diseases like schizophrenia, depression and anxiety syndrome are more common in people with toxoplasmosis, while others suggest that toxoplasmosis can influence how extroverted, aggressive or risk-inclined an individual's behaviour is.

"We've not looked at behavioural changes in people infected with toxoplasma, as that's been dealt with by previous studies," says Dr Barragan. "Instead, we've shown for the first time how the parasite behaves in the body of its host, by which I mean how it enters the brain and manipulates the host by taking over one of the brain's neurotransmitters."

In one laboratory experiment, human dendritic cells were infected with toxoplasma. After infection, the cells, which are a key component of the immune defence, started secreting the signal substance GABA. In another experiment on live mice, the team was able to trace the movement of infected dendritic cells in the body after introducing the parasite into the brain, from where it spread and continued to affect the GABA system.

GABA is a signal substance that, amongst other effects, inhibits the sensation of fear and anxiety. Disturbances of the GABA system are seen in people with depression, schizophrenia, bipolar diseases, anxiety syndrome and other mental diseases.

"For toxoplasma to make cells in the immune defence secrete GABA was as surprising as it was unexpected, and is very clever of the parasite," says Dr Barragan. "It would now be worth studying the links that exist between toxoplasmosis, the GABA systems and major public health threats."

The study was financed with a grant from the Swedish Research Council.

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Jonas M. Fuks, Romanico B. G. Arrighi, Jessica M. Weidner, Suresh Kumar Mendu, Zhe Jin, Robert P. A. Wallin, Bence Rethi, Bryndis Birnir, Antonio Barragan. GABAergic Signaling Is Linked to a Hypermigratory Phenotype in Dendritic Cells Infected by Toxoplasma gondii. PLoS Pathogens, 2012; 8 (12): e1003051 DOI: 10.1371/journal.ppat.1003051

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Monkey business: What howler monkeys can tell us about the role of interbreeding in human evolution

Dec. 7, 2012 — Did different species of early humans interbreed and produce offspring of mixed ancestry?

Recent genetic studies suggest that Neanderthals may have bred with anatomically modern humans tens of thousands of years ago in the Middle East, contributing to the modern human gene pool. But the findings are not universally accepted, and the fossil record has not helped to clarify the role of interbreeding, which is also known as hybridization.

Now a University of Michigan-led study of interbreeding between two species of modern-day howler monkeys in Mexico is shedding light on why it's so difficult to confirm instances of hybridization among primates -- including early humans -- by relying on fossil remains.

The study, published online Dec. 7 in the American Journal of Physical Anthropology, is based on analyses of genetic and morphological data collected from live-captured monkeys over the past decade. Morphology is the branch of biology that deals with the form and structure of animals and plants.

The two primate species in the study, mantled howler monkeys and black howler monkeys, diverged about 3 million years ago and differ in many respects, including behavior, appearance and the number of chromosomes they possess. Each occupies a unique geographical distribution except for the state of Tabasco in southeastern Mexico, where they coexist and interbreed in what's known as a hybrid zone.

The researchers found that individuals of mixed ancestry who share most of their genome with one of the two species are physically indistinguishable from the pure individuals of that species.

"The implications of these results are that physical features are not always reliable for identifying individuals of hybrid ancestry. Therefore, it is possible that hybridization has been underestimated in the human fossil record," said Liliana Cortés-Ortiz, an evolutionary biologist and primatologist and an assistant research scientist at the U-M Department of Ecology and Evolutionary Biology and the Museum of Zoology.

First author of the paper is Mary Kelaita, a postdoctoral fellow at the University of Texas at San Antonio's Department of Anthropology. The howler monkey study was part of Kelaita's doctoral dissertation work at U-M's Department of Anthropology.

For years, anthropologists have attempted to infer hybridization among human ancestral species based on the fossil record, which represents only a snapshot in prehistory, and have concluded that hybridization is extremely rare, according to Kelaita and Cortés-Ortiz. Given the utility of living primate models for understanding human evolution, the howler monkey study "suggests that the lack of strong evidence for hybridization in the fossil record does not negate the role it could have played in shaping early human lineage diversity," Kelaita said.

The authors conclude that the process of hybridization (defined as the production of offspring through the interbreeding between individuals of genetically distinct populations), the factors governing the expression of morphology in hybrid individuals, and the extent of reproductive isolation between species should be given further consideration in future research projects.

In their study, Kelaita and Cortés-Ortiz analyzed different types of genetic markers, from both mitochondrial and nuclear DNA, to trace the ancestry of each howler monkey they studied. The use of molecular markers made it possible to approximate the relative genetic contributions of the parental species to each hybrid.

A total of 128 hybrid individuals were detected. Kelaita and Cortés-Ortiz found that most were likely the product of several generations of hybridization or of mating between hybrids and pure individuals.

Subsequently, they performed statistical analyses on body measurements and found a large amount of morphological variation in individuals of mixed ancestry. However, when individuals were classified according to the amount of their genome they shared with each parental species, it became clear that individuals of mixed ancestry that shared most of their genome with one of the species were physically indistinguishable from the pure individuals of that species. Even individuals that were more "intermediate" in their genetic composition were not completely intermediate in their appearance.

The study is the first to assess genetic ancestry of primate hybrids inhabiting a natural hybrid zone using molecular data to explain morphological variation.

Between 1998 and 2008, the researchers sampled 135 adult howler monkeys from Tabasco, Mexico, along with 76 others from Veracruz, Campeche, Chiapas and Quintana Roo states in Mexico and Peten in Guatemala. The field team collected blood, hair and morphometric measurements from the anesthetized animals before releasing them in the same locations. Sample collection from wild monkeys was carried out in accordance with U-M's University Committee on Use and Care of Animals protocol #09319, and in collaboration with researchers at the Universidad Veracruzana in Mexico.

The animals were weighed, and 16 body-part measurements were made: trunk, tail, leg, foot, arm and hand length; chest and abdominal girth; head circumference and breadth; head, mandible and ear length; interorbital breadth; internasal distance; and testicular volume.

Howler monkeys are among the largest of New World monkeys, with male mantled howlers weighing up to 22 pounds. Fourteen species of howler monkeys are currently recognized. They are native to Central and South American forests, in addition to southeastern Mexico.

The study was supported by grants from the National Science Foundation, PROMEP-UVER Mexico, Universidad Veracruzana, and the U-M Office of the Vice President for Research, Museum of Zoology, Department of Anthropology and Rackham Graduate School.

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Mary A. Kelaita, Liliana Cortés-Ortiz. Morphological variation of genetically confirmedAlouatta Pigra×A. palliatahybrids from a natural hybrid zone in Tabasco, Mexico. American Journal of Physical Anthropology, 2012; DOI: 10.1002/ajpa.22196

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