First, glossary, helpful for specialists and lay persons alike.
Next, the naked mole rat (NMR)’s astounding features that help explain why it’s being studied intensively these days. In other words, why should we care to study the NMR‘s microbiome?
- Unlike similar sized rodents such as mice, which live at most 2 years, NMRs live into their 30s.
- Never observed to develop cancer naturally (1).
- Not observed to develop senescence (2), i.e. do not show age-related damages we see in ourselves or other animals.
- Live underground in large Eusocial colonies, the first mammals identified to do so.
- http://en.wikipedia.org/wiki/Eusociality is well-associated with insects such as bees and ants.
- Live in extensive underground burrows.
- Field studies (3) in 1957 in Kenya and Somaliland showed NMR‘s underground burrows spread out almost 40 feet (~1219 cm).
- They also extend down to about 3 feet (~90 cm) in depth.
- Modern re-imagining of NMR habitat (4). Note difference in depth. Scale here goes down to only 50cm. The actual 1957 Kenya and Somaliland field studies are likely more accurate.
- Adapted to extreme http://en.wikipedia.org/wiki/Hypoxia_%28medical%29 (low oxygen supply) (5).
- Tolerate CO2 concentrations as high as 5% (atmospheric CO2 is ~ 0.04% so NMRs tolerate 125X the CO2 that’s normal for us and other land mammals).
- Almost hairless, their slender cross-body whiskers help them navigate in the dark.
- Unlike most mammals, NMRs adapt to wide rage of temperatures (poikilothery).
- NMR skin and upper respiratory tract remarkably tolerant to irritants such as acids (6, 7).
Given it’s high-profile in recent years for its phenomenal resistance to cancer and senescence, it’s surprising there are relatively few modern studies of the NMR‘s microbiome.
- Jeff Gordon’s lab at Washington University, St. Louis, Missouri, specializes in microbiome studies.
- In 2008, this lab published a massive cross-species comparison of fecal microbiota among wild and zoo-resident mammals (8).
- NMRs housed at the St. Louis zoo were among the mammals tested.
- As is now routine for such studies, they used 16S rRNA (ribosmoal RNA) analysis to identify bacterial species and OTU (Operational Taxonomic Units). Much of microbiota identified by such molecular approaches are novel with only DNA sequence data available for comparison. Thus, OTUs represent the bulk of such microbiota.
- As for the NMR microbiome, the only thing the authors state is ‘hindgut-fermenting elephant, horse, rhinoceros, capybara, mole rat [i.e. naked mole rat] and gorilla clustered together‘ (8).
- Limitations of this study: As the glossary at the beginning suggests,16S rDNA assesses only a part of the microbiome.
Is there more data about NMR gut microbiota (see glossary for difference from microbiome)?
- Yes, in a few older studies from the 1950s and the 1990s. Stand alone, not comparisons.
- Since NMRs live in protein-poor environments, they may use their endosymbionts as a protein source (9).
- NMR have http://en.wikipedia.org/wiki/Hindgut_fermentation, unlike foregut fermenters like ruminants (e.g. cows).
- A diverse population of hindgut (cecum and colon) protists (protozoa), bacteria and fungi ferment and help digest the NMR‘s food (10).
- NMR‘s feces contain the bacteria and protists it needs to digest cellulose (11).
- Weaning NMR pups make unique sounds when they beg for feces from adults (12). This suggests it’s really important for them to acquire adult fecal microbes.
- Not just any fecal pellets but rather special ones called cecotropes, soft, partially digested fecal pellets meant to be reingested. Other hindgut fermenting rodents such as guinea pigs also produce and reingest cecotropes.
- Cecotropes replenish cecal microbiota (found in the cecum) in older NMRs and serve as seed microbiota in pups.
- Such cecal microbiota produce essential volatile fatty acids (Short-chain fatty acids, SCFA), amino acids and vitamins. In short they support the NMR‘s basic metabolic needs (11, 13).
Examples of cecal protists isolated from NMR captured in Kenya and Somaliland in the 1950s (12).
Summary of the data (14):
- Many protists (protozoa) were found in NMR fecal pellets.
- Not similar in NMR from Kenya and Somaliland.
- For example, Entamoeba and Giardia species were observed only in Somaliland NMR.
- This suggests local environment-based specialized host-symbiont adaptation between NMR and their microbes.
- An as-yet unpublished study (16) from the University of Leipzig, Germany, compared the fecal microbiota of NMR from the wild and in captivity.
- Identified by culture under aerobic and anaerobic conditions.
- Culture isolates subjected to Matrix Laser Desorption Ionization Time-of-Flight (MALDI-TOF) mass spectrometry.
- They found the bacterium Bacillus megaterium only in NMR living in the wild.
Bottomline: extensive microbiota studies of NMR are needed. Not just bacteria but also fungi, protists, viruses. Not just gut but also oral, lung and genital mucoase, and skin. Only then will we begin to understand how their microbiota contribute to their unique longevity, and their observed protection from inflammation and stress as well as their resistance to cancer.
- Tian, Xiao, et al. “High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat.” Nature 499.7458 (2013): 346-349. http://grtc.ucsd.edu/curr_lit_fa13/101113_HyaluronanPaper.pdf
- Buffenstein, Rochelle. “Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species.” Journal of Comparative Physiology B 178.4 (2008): 439-445.
- Hill, WC Osman, et al. “Field and laboratory studies on the naked mole rat, Heterocephalus glaber.” Proceedings of the Zoological Society of London. Vol. 128. No. 4. Blackwell Publishing Ltd, 1957.
- Larson, John, and Thomas J. Park. “Extreme hypoxia tolerance of naked mole-rat brain.” Neuroreport 20.18 (2009): 1634-1637.
- Park, Thomas J., et al. “Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber).” PLoS biology 6.1 (2008): e13. http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0060013#pbio-0060013-g008
- Smith, Ewan St John, et al. “The molecular basis of acid insensitivity in the African naked mole-rat.” Science 334.6062 (2011): 1557-1560.
- Ley, Ruth E., et al. “Evolution of mammals and their gut microbes.” Science 320.5883 (2008): 1647-1651. http://obs.rc.fas.harvard.edu/turnbaugh/Papers/Ley_Science2008.pdf
- Dyer, B. D. “A hypothesis about the significance of symbionts as a source of protein in the evolution of eusociality in naked mole rats.” Symbiosis 24.3 (1998): 369-383.
- Buffenstein, Rochelle, and Shlomo Yahav. “The effect of diet on microfaunal population and function in the caecum of a subterranean naked mole-rat, Heterocephalus glaber.” British journal of nutrition 65.02 (1991): 249-258.
- PORTER, ANNIE. “Morphology and affinities of entozoa and endophyta of the naked mole rat Heterocephalus glaber.” Proceedings of the Zoological Society of London. Vol. 128. No. 4. Blackwell Publishing Ltd, 1957.
- Sherman, Paul W., Jennifer UM Jarvis, and Richard D. Alexander. “Biology of the Naked Mole-rat.” Monographs in behavior and ecology (USA) (1991).
- Suckow, Mark A., Karla A. Stevens, and Ronald P. Wilson, eds. The laboratory rabbit, guinea pig, hamster, and other rodents. Academic Press, 2011.
- De Graaff, G. “On the parasites associated with the Bathyergidae.” Koedoe 7 (1964): 113-123. http://www.koedoe.co.za/index.php/koedoe/article/viewFile/806/911
- Chapter 45. Naked Mole Rat. Pages 1055- 1074. Authors: Rochelle Buffenstein, Thomas Park, Martha Hanes, and James E. Artwohl. Suckow, Mark A., Karla A. Stevens, and Ronald P. Wilson, eds. The laboratory rabbit, guinea pig, hamster, and other rodents. Academic Press, 2011.