Category Archives: microbiome

The Microbial Anthropocene

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Over the last decade or so, geologists and ecologists have begun to talk about planet earth entering a new geologic period called the Anthropocene, defined as the period when humans became the driving force of change on planet Earth. Debates continue on when the Anthropocene begins; sometime in the late 18th century when the industrial age is underway with the first steam engines, new products appear like plastic that persist in geology, and in medicine, Jenner begins his work on vaccines in the 1790s, would make sense.  I suggest that this also marks the beginning of the microbial Anthropocene — when humans become a driving force in microbial evolution.

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Microbiology of the Anthropocene (Gillings and Paulson, 2013). Note the logarithmic time scale.

The graphic above is eye-opening. The Anthropocene is apparent in every level of microbial ecology examined. It is a good reminder that human intervention in microbial evolution goes far beyond infectious disease.

Perhaps most stunning message this graphic brought to me is the logarithmic nature of change. It finally dawned on me looking at this graphic that it also reflects the periods of epidemiological transition theory (ETT). The hunter-gatherer period correlates with the Pleistocene, then the first transition to the farmer-urban period (of epidemics) correlates with the Holocene, and the second transition to the modern third epidemiological phase characterized by longer lifespans and chronic disease is the Anthropocene.  Finally, the time scale of the epidemiologic transitions makes some sense. The logarithmic scale may not bode well for the speed of future transitions.

The changes of the Anthropocene filter down through all living and non-living things. Among living things, there are winners and losers: species whose range and differentiation expands and others are driven to extinction. We can see this on a huge scale in the ocean where we have coral bleaching caused by loss of microbial symbionts, while there is an increasing incidence of toxic blooms and an enlarging dead zone in the Gulf of Mexico both caused by an overgrowth of some microbial species. With each transition, natural selection seems to go into overdrive until a new equilibrium is established (Gilling and Paulsen, 2).

Michael Gillings and Ian Paulsen identified several areas of microbial evolution and ecology impacted during the Anthropocene. The strong selective pressure antibiotics have exerted on infectious agents is the most commonly discussed risk in modern medical microbiology. Changes in the human microbiome are most closely related to diet changes (another feature of the Anthropocene), but our normal flora is also collateral damage of antimicrobial treatment. We often overlook that most antibiotics consumed by humans and livestock are washed through our bodies into the watershed where they alter the microbial ecology of entire ecosystems. Antimicrobial therapy began long before traditional modern antibiotics; mercury was used in medieval medicine to treat syphilis, leprosy and as a topical treatment for lice. Arsenic is still used to poison pests like rats. These early antimicrobials prompted the increase and spread of mercury and arsenic resistance in a wide variety of pathogens and environmental bacteria.

Industrial and agricultural practices have involved bacteria in changes to the global biogeochemistry and played a major role in climate change. The spread of industrialized agriculture has increased the methane production from (bacteria in) livestock, rice patties, and landfills. Crop rotations with legumes with their nitrogen-fixing symbionts increase the agricultural output of the land but in doing so the symbionts have altered the global nitrogen cycle. Gillings and Paulsen observed that the combined effect of burning fossil fuels, cultivating legumes, and industrial nitrogen fixation in fertilizer now accounts for about 45% of global nitrogen fixation. Agriculture on an industrial scale has impacted soil microbiology to the point where it has altered the carbon and nitrogen cycle of the entire planet. Elevated levels of methane and carbon dioxide do more than raise just the global temperature. While some have breathed a sigh of relief that the oceans have acted as a carbon sink, it has not been without cost. An acidic ocean is a price we pay for the carbon sink.  The drop in marine pH will affect all microbial communities down to the depths of the abyss. Coral bleaching due to a loss of their microbial symbionts is just one of the most obvious outcomes.

Disease emergence and dispersal has been more of a mixed bag. New diseases get a great deal of attention but with the exception of HIV, they are not worse than the “age of epidemics”  (plague, typhoid fever, yellow fever, etc.).   Vaccines have still amounted to an overall decrease in infectious disease deaths. The three worst diseases to emerge during the Anthropocene are cholera, influenza, and HIV/AIDS. The greatest concerns today are the speed of dispersal for antibiotic resistant strains of old foes and development of new vaccines. Still, though, there are possibly more infectious organisms than ever.  We have driven only two viruses to extinction — smallpox and rinderpest — while new zoonotic diseases emerge at a steady clip.

Completely synthetic microbes created in a laboratory may well eventually be the primary hallmark of the Anthropocene. We are on the verge of being there now and there are an uncountable number of engineered microbes that produce a variety of products from biofuels to drugs. It will be up to us to manage the use of a technology capable of resurrecting a long-extinct bacterial strain or virus.

Do we really think we are smart enough to manage the tsunami of change occurring the microbial world?

 


References

Gillings, M. R., & Paulsen, I. T. (2013). Microbiology of the Anthropocene. Anthropocene, 5, 1-8. http://doi.org/10.1016/j.ancene.2014.06.004

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The Pathogen Buzz of 2016

by Michelle Ziegler

Altmetrics recently released the Top 100 scholarly articles list for the year (captured on 15 Nov 2016). Their ranking captures the public discussion on academic articles judged by shares of the online edition, news articles, blog posts and tweets that include the digital object identifier code (doi). (So if you want to improve the Altmetrics number of your papers make sure that all blog posts/tweets/news articles have the doi somewhere.) Note that generating discussion is not the same as being the best papers produced. At least one one this list, on ‘Patient 0’ HIV-1,  seemed to generate a fair amount of complaints.

Overall, the list was dominated by medical and health science (49) and biological science (14), altogether being 63% of the top 100 articles. Some of the other categories are a little vague, such as physical science (6) vs. earth and environmental science (6) vs. material science (1). History and archaeology combined to produce only six of the top 100 and one of them, on the ‘Tully monster’, really should be paleontology (or biology?). We also have to keep in mind that Altmetrics misses most of the humanities journals. The Altmetric scores in the top hundred have also approximately doubled between 2014 and 2016. The lowest score in 2016 is 1605 and the lowest score in 2014 was only 746.

One highlight this year is that 47% of the top 100 were either freely available or open access. I noticed about midway through this past year that papers expected to get a lot of attention were often freely available or open access. The difference between freely available vs open access may be whether or not the authors had to pay for the open availability (?). I wonder if the freely available remain free forever, or only until the news dies down?

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Zika vector Aedes aegypti (Courtesy of CDC/Public Health Image Library #9261)

When it comes to pathogens, this year’s list comes with the distinctive buzz of a mosquito, Aedes aegypti, carrying this year’s emerging infectious disease, the Zika virus. Of the twelve papers directly related to infection, six are on Zika. Looking at the 2015 list, it’s clear that Zika put pathogens in the news this year. There are hardly no pathogen related papers in the 2015 list and in 2014, there were only five  – four on ebola and one on ancient Yersinia pestis. So clearly Zika has made a far bigger splash than even the much more lethal ebola.

Pathogens in the 2016 Top 100:

6. Rasmussen, S. A., Jamieson, D. J., Honein, M. A., & Petersen, L. R. (2016). Zika virus and birth defects—reviewing the evidence for causality. New England Journal of Medicine, 374(20), 1981-1987. DOI: 10.1056/nejmsr1604338

17. Zipperer, A., Konnerth, M. C., Laux, C., Berscheid, A., Janek, D., Weidenmaier, C., … & Willmann, M. (2016). Human commensals producing a novel antibiotic impair pathogen colonization. Nature, 535(7613), 511-516. DOI: 10.1001/jama.2016.0287

19. Singer, M., Deutschman, C. S., Seymour, C. W., Shankar-Hari, M., Annane, D., Bauer, M., … & Hotchkiss, R. S. (2016). The third international consensus definitions for sepsis and septic shock (sepsis-3). Jama, 315(8), 801-810.17. DOI: 10.1001/jama.2016.0287

20. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., … & Vizjak, A. (2016). Zika virus associated with microcephaly. New England Journal of Medicine, 374(10), 951-958. DOI: doi/10.1056/NEJMoa1600651

 
25. Miranda, R. C., & Schaffner, D. W. (2016). Longer contact times increase cross-contamination of Enterobacter aerogenes from surfaces to food. Applied and Environmental Microbiology, 82(21), 6490-6496. DOI:10.1128/aem.01838-1620.

31. McGann, P., Snesrud, E., Maybank, R., Corey, B., Ong, A. C., Clifford, R., … & Schaecher, K. E. (2016). Escherichia coli Harboring mcr-1 and blaCTX-M on a Novel IncF Plasmid: First report of mcr-1 in the USA. Antimicrobial agents and chemotherapy. DOI: 10.1128/aac.01103-16

 
37. Cao-Lormeau, V. M., Blake, A., Mons, S., Lastère, S., Roche, C., Vanhomwegen, J., … & Vial, A. L. (2016). Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. The Lancet, 387(10027), 1531-1539. DOI: 10.1016/s0140-6736(16)00562-6

46. Worobey, M., Watts, T. D., McKay, R. A., Suchard, M. A., Granade, T., Teuwen, D. E., … & Jaffe, H. W. (2016). 1970s and ‘Patient 0’HIV-1 genomes illuminate early HIV/AIDS history in North America. Nature, 539(7627), 98-101. DOI: 10.1038/nature19827

49. Fauci, A. S., & Morens, D. M. (2016). Zika virus in the Americas—yet another arbovirus threat. New England Journal of Medicine, 374(7), 601-604. DOI: 10.1056/nejmp1600297

54. Tang, H., Hammack, C., Ogden, S. C., Wen, Z., Qian, X., Li, Y., … & Christian, K. M. (2016). Zika virus infects human cortical neural progenitors and attenuates their growth. Cell stem cell, 18(5), 587-590. DOI: 10.1016/j.stem.2016.02.016

86. Liu, Y. Y., Wang, Y., Walsh, T. R., Yi, L. X., Zhang, R., Spencer, J., … & Yu, L. F. (2016). Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. The Lancet Infectious Diseases, 16(2), 161-168.54. DOI: 10.1016/S1473-3099(15)00424-7

92. Brasil, P., Pereira, Jr, J. P., Raja Gabaglia, C., Damasceno, L., Wakimoto, M., Ribeiro Nogueira, R. M., … & Calvet, G. A. (2016). Zika virus infection in pregnant women in Rio de Janeiro—preliminary report. New England Journal of Medicine. DOI: 10.1056/NEJMoa1602412

Before we leave the buzz of 2016, we have to mention this year also saw the passing of Dr. Donald Henderson (1928-2016) who led the effort to eradicate smallpox. Henderson died in August; his obituary from the New York Times can be found here.

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Henderson administering a smallpox vaccine in about 1972 (WHO).