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Diversity and novelty of the gut microbial community of an herbivorous rodent (Neotoma bryanti)

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Abstract

Mammalian herbivores host diverse microbial communities to aid in fermentation and potentially detoxification of dietary compounds. However, the microbial ecology of herbivorous rodents, especially within the largest superfamily of mammals (Muroidea) has received little attention. We conducted a preliminary inventory of the intestinal microbial community of Bryant’s woodrat (Neotoma bryanti), an herbivorous Muroidea rodent. We collected woodrat feces, generated 16S rDNA clone libraries, and obtained sequences from 171 clones. Our results demonstrate that the woodrat gut hosts a large number of novel microorganisms, with 96% of the total microbial sequences representing novel species. These include several microbial genera that have previously been implicated in the metabolism of plant toxins. Interestingly, a comparison of the community structure of the woodrat gut with that of other mammals revealed that woodrats have a microbial community more similar to foregut rather than hindgut fermenters. Moreover, their microbial community was different to that of previously studied herbivorous rodents. Therefore, the woodrat gut may represent a useful resource for the identification of novel microbial genes involved in cellulolytic or detoxification processes.

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References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Alvarez PJJ, Vogel TM (1991) Substrate interactions of benzene, toluene, and para-xylene during microbial degradation by pure cultures and mixed culture aquifer slurries. Appl Environ Microbiol 57(10):2981–2985

    PubMed  CAS  Google Scholar 

  • Barrangou R, Azcarate-Peril MA, Duong T, Conners SB, Kelly RM, Klaenhammer TR (2006) Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc Natl Acad Sci 103(10):3816–3821

    Article  PubMed  CAS  Google Scholar 

  • Bauer JE, Capone DG (1988) Effects of co-occuring aromatic hydrocarbons on degradation of individual polycyclic aromatic hydrocarbons in marine sediment slurries. Appl Environ Microbiol 54(7):1649–1655

    PubMed  CAS  Google Scholar 

  • Brooks SPJ, McAllister M, Sandoz M, Kalmokoff ML (2003) Culture-independent phylogenetic analysis of the faecal flora of the rat. Can J Microbiol 49:589–601

    Article  PubMed  CAS  Google Scholar 

  • Carleton MD (1973) A survey of gross stomach morphology in New World Cricetinae (Rodentia, Muroidea), with comments on functional interpretations. Museum of Zoology, University of Michigan, Ann Arbor

    Google Scholar 

  • Costello EK, Gordon JI, Secore SM, Knight R (2010) Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J 4:1375–1385

    Article  PubMed  CAS  Google Scholar 

  • Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Ann Rev Ecol Evol Syst 36:169–185

    Article  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006a) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W394–W399

    Article  PubMed  CAS  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006b) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  PubMed  CAS  Google Scholar 

  • Forsberg CW, Cheng KJ, White BA (1997) Polysaccharide degradation in the rumen and large intestine. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall, New York, pp 319–379

    Google Scholar 

  • Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–287

    Article  CAS  Google Scholar 

  • Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27

    Article  PubMed  CAS  Google Scholar 

  • Hespell RB, Aiken DE, Dehority BA (1997) Bacteria, fungi, and protozoa in the rumen. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman & Hall, New York, pp 59–141

    Google Scholar 

  • Hiura T, Hashidoko Y, Kobayashi Y, Tahara S (2010) Effective degradation of tannic acid by immobilized rumen microbes of a sika deer (Cervus nippon yesoensis) in winter. Anim Feed Sci Technol 155:1–8

    Article  CAS  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20(14):2317–2319

    Article  PubMed  CAS  Google Scholar 

  • Hyder PW, Fredrickson EL, Estell RE, Tellez M, Gibbens RP (2002) Distribution and concentration of total phenolics, condensed tannins, and nordihydroguaiaretic acid (NDGA) in creosotebush (Larrea tridentata). Biochem Syst Ecol 30:905–912

    Article  CAS  Google Scholar 

  • Jones RJ, Megarrity RG (1986) Successful transfer of DHP-degrading bacteria from Hawaiian goats to Australian ruminants to overcome the toxicity of Leucaena. Aust Vet J 63(8):259–262

    Article  PubMed  CAS  Google Scholar 

  • Karasov WH (1989) Nutritional bottleneck in a herbivore, the desert wood dar (Neotoma lepida). Physiol Zool 62:1351–1382

    Google Scholar 

  • Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton

    Google Scholar 

  • Kobayashi Y (2006) Inclusion of novel bacteria in rumen microbiology: need for basic and applied science. Anim Sci J 77(4):375–385

    Article  CAS  Google Scholar 

  • Kotze SH, Van Der Merwe EL, Bennett NC, O’Riain MJ (2010) The comparative anatomy of the abdominal gastrointestinal tract of six species of African mole-rats (Rodentia, Bathyergidae). J Morphol 271(1):50–60

    Article  PubMed  Google Scholar 

  • Landry SO Jr (1970) The Rodentia as omnivores. Q Rev Biol 45:351–372

    Article  PubMed  Google Scholar 

  • Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848

    Article  PubMed  CAS  Google Scholar 

  • Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651

    Article  PubMed  CAS  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(2):8228–8235

    Article  PubMed  CAS  Google Scholar 

  • Lozupone C, Lladser M, Knights D, Stombaugh J, Knight R (2010) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172

    Article  PubMed  Google Scholar 

  • Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69(11):6816–6824

    Article  PubMed  CAS  Google Scholar 

  • Ludwig W, Strunk O, Klugbauer S, Weizenegger M, Neumaier J, Bachleither M, Schleifer KH (1998) Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554–568

    Article  PubMed  CAS  Google Scholar 

  • Luo C, Xie S, Sun W, Li X, Cupples AM (2009) Identification of a novel toluene-degrading bacterium from the candidate phylum TM7, as determined by DNA stable isotope probing. Appl Environ Microbiol 75(13):4644–4647

    Article  PubMed  CAS  Google Scholar 

  • Marshall AJ, Cannon CH, Leighton M (2009) Competition and niche overlap between gibbons (Hylobates albibarbis) and other frugivorous vertebrates in Gunung Palung National Park, West Kalimantan, Indonesia. In: Whittaker D, Lappan S (eds) The Gibbons. Developments in primatology: progress and prospects. Springer, New York, pp 161–188

    Google Scholar 

  • McSweeney CS, Mackie RI (1997) Gastrointestinal detoxification and digestive disorders in ruminant animals. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall, New York

    Google Scholar 

  • Meyer MW, Karasov WH (1989) Antiherbivore chemistry of Larrea tridentata: effects on woodrat (Neotoma lepida) feeding and nutrition. Ecology 70:953–961

    Article  Google Scholar 

  • Musser GG, Carleton MD (2005) Order Rodentia. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore, pp 745–752

    Google Scholar 

  • Ozutsumi Y, Hayashi H, Sakamoto M, Itabashi H, Benno Y (2005) Culture-independent analysis of fecal microbiota in cattle. Biosci Biotechnol Biochem 69:1793–1797

    Article  PubMed  CAS  Google Scholar 

  • Patel TR, Jure KG, Jones GA (1981) Catabolism of phloroglucinol by the rumen anaerobe Coprococcus. Appl Environ Microbiol 42(6):1010–1017

    PubMed  CAS  Google Scholar 

  • Pope PB, Denman SE, Jones M, Tringe SG, Barry K, Malfatti SA, McHardy AC, Cheng J-F, Hugenholtz P, McSweeney CS, Morrison M (2010) Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores. Proc Natl Acad Sci 107:14793–14798

    Article  PubMed  CAS  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490

    Article  PubMed  Google Scholar 

  • Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Ann Rev Microbiol 57:369–394

    Article  CAS  Google Scholar 

  • Rawls JF, Mahowald MA, Ley RE, Gordon JI (2006) Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127:423–433

    Article  PubMed  CAS  Google Scholar 

  • Rosenthal GA, Berenbaum MR (1991) Herbivores: their interactions with secondary plant metabolites, vol. 1. Academic, San Diego

    Google Scholar 

  • Shimada T, Saitoh T, Sasaki E, Nishitani Y, Osawa R (2006) Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins. J Chem Ecol 32:1165–1180

    Article  PubMed  CAS  Google Scholar 

  • Skopec MM, Haley S, Torregrossa A-M, Dearing MD (2008) An oak (Quercus agrifolia) specialist (Neotoma macrotis) and a sympatric generalist (Neotoma lepida) show similar intakes and digestibilities of oak. Physiol Biochem Zool 81:426–433

    Article  PubMed  Google Scholar 

  • Smith GS (1992) Toxification and detoxification of plant compounds by ruminants: an overview. J Range Manage 45(1):25–30

    Article  Google Scholar 

  • Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in Bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  • Stevens CE, Hume ID (2004) Comparative physiology of the vertebrate digestive system, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Sundset MA, Barboza PS, Green TK, Folkow LP, Blix AS, Mathiesen SD (2010) Microbial degradation of usnic acid in the reindeer rumen. Naturwissenschaften 97:273–278

    Article  PubMed  CAS  Google Scholar 

  • Van Soest PJ (1994) Nurtitional ecology of the ruminant. Cornell University Press, Ithaca

    Google Scholar 

  • Wang Q, Garrity GM, Tiedja JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinforma 7:57

    Article  Google Scholar 

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Acknowledgments

We thank J. Malenke and J. Varner for animal collection, and K. Smith and D. Dunn for help with 16S rDNA sequencing. We also thank Kerrin Grant and one other anonymous reviewer for helping to improve the manuscript. This study was supported by grants from SICB, Sigma Xi, Southwest Association of Naturalists, American Museum of Natural History, and NSF GRFP to K.D.K and NSF IOS 0817527 to M.D.D.

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Correspondence to Kevin D. Kohl.

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Kohl, K.D., Weiss, R.B., Dale, C. et al. Diversity and novelty of the gut microbial community of an herbivorous rodent (Neotoma bryanti). Symbiosis 54, 47–54 (2011). https://doi.org/10.1007/s13199-011-0125-3

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  • DOI: https://doi.org/10.1007/s13199-011-0125-3

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