Skip to main content

Advertisement

Log in

Supplementing Blends of Sugars, Amino Acids, and Secondary Metabolites to the Diet of Termites (Reticulitermes flavipes) Drive Distinct Gut Bacterial Communities

  • Notes and Short Communications
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Although it is well known that diet is one of the major modulators of the gut microbiome, how the major components of diet shape the gut microbial community is not well understood. Here, we developed a simple system that allows the investigation of the impact of given compounds as supplements of the diet on the termite gut microbiome. The 16S rRNA pyrosequencing analysis revealed that feeding termites different blends of sugars and amino acids did not majorly impact gut community composition; however, ingestion of blends of secondary metabolites caused shifts in gut bacterial community composition. The supplementation of sugars and amino acids reduced the richness significantly, and sugars alone increased the evenness of the gut bacterial community significantly. Secondary metabolites created the most dramatic effects on the microbial community, potentially overriding the effect of other types of compounds. Furthermore, some microbial groups were stimulated specifically by particular groups of compounds. For instance, termites fed with secondary metabolites contained more Firmicutes and Spirochaetes compared to the other treatments. In conclusion, our results suggest that the termite (Reticulitermes flavipes) can be used as a simple and effective system to test the effects of particular chemical compounds in modulating the gut microbiome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, Wu GD et al (2013) Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One 8:e66019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ et al (2014) Characterisation of the faecal bacterial community in adult and elderly horses fed a high fibre, high oil or high starch diet using 454 pyrosequencing. PLoS One 9:e87424

    Article  PubMed  PubMed Central  Google Scholar 

  4. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Salonen A, de Vos WM (2014) Impact of diet on human intestinal microbiota and health. Annu Rev Food Sci Technol 5:239–262

    Article  CAS  PubMed  Google Scholar 

  6. Etxeberria U, Fernández-Quintela A, Milagro FI, Aguirre L, Martínez JA, Portillo MP (2013) Impact of polyphenols and polyphenol-rich dietary sources on gut microbiota composition. J Agric Food Chem 61:9517–9533

    Article  CAS  PubMed  Google Scholar 

  7. Huang X-F, Bakker M, Judd T, Reardon K, Vivanco J (2013) Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microb Ecol 65:531–536

    Article  PubMed  Google Scholar 

  8. Husseneder C, Berestecky JM, Grace JK (2009) Changes in composition of culturable bacteria community in the gut of the formosan subterranean termite depending on rearing conditions of the host. Ann Entomol Soc Am 102:498–507

    Article  Google Scholar 

  9. Sluiter JB, Ruiz RO, Scarlata CJ, Sluiter AD, Templeton DW (2010) Compositional analysis of lignocellulosic feedstocks. 1. Review and description of methods. J Agric Food Chem 58:9043–9053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Boucias DG, Cai Y, Sun Y, Lietze V-U, Sen R, Raychoudhury R et al (2013) The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition. Mol Ecol 22:1836–1853

    Article  CAS  PubMed  Google Scholar 

  11. Wertz JT, Kim E, Breznak JA, Schmidt TM, Rodrigues JLM (2012) Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Appl Environ Microbiol 78:1544–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tanaka H, Aoyagi H, Shiina S, Doudou Y, Yoshimura T, Nakamura R et al (2006) Influence of the diet components on the symbiotic microorganisms community in hindgut of Coptotermes formosanus Shiraki. Appl Microbiol Biotechnol 71: 907-917

  13. Sethi A, Slack JM, Kovaleva ES, Buchman GW, Scharf ME (2013) Lignin-associated metagene expression in a lignocellulose-digesting termite. Insect Biochem Mol Biol 43:91–101

    Article  CAS  PubMed  Google Scholar 

  14. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ottesen EA, Hong JW, Quake SR, Leadbetter JR (2006) Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314:1464–1467

    Article  CAS  PubMed  Google Scholar 

  16. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009). Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl Environ Microbiol 75: 7537–7541

  17. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of pcr amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Quince C, Lanzen A, Davenport R, Turnbaugh P (2011) Removing noise from pyrosequenced amplicons. BMC Bioinf 12:38

    Article  Google Scholar 

  19. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Köhler T, Dietrich C, Scheffrahn RH, Brune A (2012) High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl Environ Microbiol 78:4691–4701

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are grateful for funding from the Sustainable Bioenergy Development Center at Colorado State University. We are thankful to all members in the Vivanco laboratory for constructive and invaluable comments on the manuscript. We are also thankful to Dr. Tiffany Weir, Dr. Dan Manter, Dr. Matt Bakker, Dr. Ranjan Srivastava, Dr. Luo Bjostad, and Mr. Charlie Vollmer for reviewing the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jorge M. Vivanco.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Xing-Feng Huang and Jacqueline M. Chaparro contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(XLSX 35 kb)

Table S2

(XLSX 22 kb)

Table S3

(XLSX 11 kb)

Supplemental Figure 1

Dilution-to-extinction PCR of cDNA from termite guts amplified with Verrucomicrobia, Spirochaetes, and general Bacteria (16S rRNA) specific primers. The cDNA pool used for pyrosequencing was diluted to 1/4, 1/8, 1/16, 1/32, 1/64, 1/128, 1/256. The PCR was conducted with 3 biological replicates with similar results. The images represent the results of one replicate. The bands of Spirochaetes group at dilutions of 1/32, 1/64, and 1/128 were similar to the bands of general bacteria at dilutions of 1/64, 1/128, and 1/256, respectively. Meanwhile, the bands of Verrucomicrobia group at dilutions of 1/4, 1/8, and 1/16 were similar to the bands of general bacteria at dilutions of 1/64, 1/128, and 1/256, respectively. (JPG 20 kb)

High resolution image (TIF 1960 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, XF., Chaparro, J.M., Reardon, K.F. et al. Supplementing Blends of Sugars, Amino Acids, and Secondary Metabolites to the Diet of Termites (Reticulitermes flavipes) Drive Distinct Gut Bacterial Communities. Microb Ecol 72, 497–502 (2016). https://doi.org/10.1007/s00248-016-0792-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0792-y

Keywords

Navigation