Patterns of [FeFe] hydrogenase diversity in the gut microbial communities of lignocellulose-feeding higher termites

Applied and Environmental Microbiology

Volumn 78, Issue 15, 2012, Pages 5368-5374

  Ballor, Nicholas R ^a   Leadbetter, Jared R ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

[FEFE]HYDROGENASES; DEGENERATE PRIMERS; GUT MICROBES; HYDROGENASES; METAGENOMES; MICROBIAL COMMUNITIES; TERMITE GUT;

BACTERIA; CLONING; DEGRADATION; ECOSYSTEMS; METABOLISM; PHYSIOLOGY;

HYDROGEN;

HYDROGEN; HYDROGENASE; IRON HYDROGENASE; IRON SULFUR PROTEIN; LIGNIN; LIGNOCELLULOSE; PRIMER DNA;

CELLULOSE; DIGESTIVE SYSTEM; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; FEEDING; HYDROGEN; LIGNIN; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; PHYLOGENETICS; PHYSIOLOGY; TERMITE;

ANIMAL; ARTICLE; BACTERIUM; BIOLOGICAL MODEL; COSTA RICA; DNA SEQUENCE; ENZYMOLOGY; GASTROINTESTINAL TRACT; GENETIC VARIABILITY; GENETICS; ISOPTERA; METABOLISM; METAGENOME; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; STATISTICAL MODEL;

ANIMALS; BACTERIA; BASE SEQUENCE; CLONING, MOLECULAR; COSTA RICA; DNA PRIMERS; GASTROINTESTINAL TRACT; GENETIC VARIATION; HYDROGEN; HYDROGENASE; IRON-SULFUR PROTEINS; ISOPTERA; LIGNIN; LIKELIHOOD FUNCTIONS; METAGENOME; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SEQUENCE ANALYSIS, DNA;

AMITERMES; CRYPTOCERCUS PUNCTULATUS; GNATHAMITERMES; ISOPTERA; MICROCEROTERMES; NASUTITERMES; PROTOZOA; TERMITIDAE;

EID: 84866156925     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.08008-11     Document Type: Article

References (51)

1. Anderson KE, et al. 2012. Highly similar microbial communities are shared among related and trophically similar antspecies. Mol. Ecol. 21: 2282-2296.
2. Ballor NR, Leadbetter JR. 2012. Analysis of extensive [FeFe] hydrogenase gene diversity within the gut microbiota of insects representing five families of Dictyoptera. Microb. Ecol. 63:586-595.
3. 2-rich termite gut. Microb. Ecol. 63:282-294.
4. Berlanga M, Paster BJ, Guerrero R. 2007. Coevolution of symbiotic spirochete diversity in lower termites. Int. Microbiol. 10:133-139.
5. Boyd ES, Hamilton TL, Spear JR, Lavin M, Peters JW. 2010. [FeFe]- hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism. ISME J. 4:1485-1495.
6. Boyd ES, Spear JR, Peters JW. 2009. [FeFe] hydrogenase genetic diversity provides insight into molecular adaptationin a saline microbial mat community. Appl. Environ. Microbiol. 75:4620-4623.
7. Brauman A, Kane MD, Labat M, Breznak JA. 1992. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384-1387.
8. Breznak JA. 2000. Ecology of prokaryotic microbes in the guts of woodand litter-feeding termites, p 209-231. In AbeT, Bignell DE, Higashi M (ed), Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Boston, MA.
9. Breznak JA. 1982. Intestinal microbiota of termites and other xylophagous insects. Annu. Rev. Microbiol. 36:323-343.
10. Breznak JA, Brune A. 1994. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Entomol. 39:453-487.
11. 2 by termite gut microbes. Appl. Environ. Microbiol. 52:623-630.
12. Brune A. 2006. Symbiotic associations between termites and prokaryotes, p 439-474. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (ed), The prokaryotes, 3rd ed, vol 1. Springer Science+Business Media, LLC, New York, NY.
13. Brune A. 1998. Termite guts: the world's smallest bioreactors. Trends Biotechnol. 16:16-21.
14. Brune A, Friedrich M. 2000. Microecology of the termite gut: structure and function on a microscale. Curr. Opin. Microbiol. 3:263-269.
15. Brune A, Kühl M. 1996. pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J. Insect Physiol. 42:1121-1127.
16. Clark JW, Hossain S, Burnside CA, Kambhampati S. 2001. Coevolution between a cockroach and its bacterial endosymbiont:a biogeographical perspective. Proc. Biol. Sci. 268:393-398.
17. Cleveland LR. 1923. Correlation between the food and morphology of termites and the presence of intestinal protozoa. Am. J. Epidemiol. 3:444-461.
18. Ebert A, Brune A. 1997. Hydrogen concentration profiles at the oxicanoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl. Environ. Microbiol. 63:4039-4046.
19. Eggleton P. 2006. The termite gut habitat: its evolution and co-evolution, p 373-404. In König H, Varma A (ed), Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, Germany.
20. Felsenstein J. 1989. PHYLIP-phylogeny inference package (version 32). Cladistics 5:164-166.
21. Hongoh Y, et al. 2005. Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl. Environ. Microbiol. 71:6590-6599.
22. Inoue J-I, Saita K, Kudo T, Ui S, Ohkuma M. 2007. Hydrogen production by termite gut protists: characterization of iron hydrogenases of parabasalian symbionts of the termite Coptotermes formosanus. Eukaryot. Cell 6:1925-1932.
23. Inward D, Beccaloni G, Eggleton P. 2007. Death of an order: a comprehensive molecular phylogenetic study confirms thattermites are eusocial cockroaches. Biol. Lett. 3:331-335.
24. Inward DJG, Vogler AP, Eggleton P. 2007. A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol. Phylogenet. Evol. 44:953-967.
25. Kambhampati S, Eggleton P. 2000. Taxonomy and phylogeny of termites, p 1-23. In Abe T, Bignell DE, HigashiM(ed), Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Boston, MA.
26. Leadbetter JR, Breznak JA. 1996. Physiological ecology of Methanobrevibacter cuticularis sp nov and Methanobrevibactercurvatus sp nov, isolated from the hindgut of the termite Reticulitermes flavipes. Appl. Environ. Microbiol. 62:3620-3631.
27. Legendre F, et al. 2008. The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers:implications for evolution of the worker and pseudergate castes, and foraging behaviors. Mol. Phylogenet. Evol. 48:615-627.
28. Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T. 2003. Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol. Biol. Evol. 20:907-913.
29. Lozupone C, Hamady M, Knight R. 2006. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371. doi:10.1186/1471-2105-7-371.
30. Magurran AE. 1988. Ecological diversity and its measurement. Princeton University Press, Princeton, NJ.
31. Matson EG, Ottesen EA, Leadbetter JR. 2007. Extracting DNA from the gut microbes of the termite (Zootermopsis nevadensis). J. Vis. Exp. 2007(4): 195. doi:10.3791/195.
32. Miyata R, et al. 2007. Influence of feed components on symbiotic bacterial community structure in the gut of the wood-feeding higher termite Nasutitermes takasagoensis. Biosci. Biotechnol. Biochem.71:1244-1251.
33. Noda S, et al. 2007. Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), theirhosts, and their bacterial endosymbionts. Mol. Ecol. 16:1257-1266.
34. Noirot C. 1995. The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. I. Lower termites. Ann. Soc. Entomol. Fr. 31:197-226.
35. Noirot C. 2001. The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. II. Higher termites (Termitidae). Ann. Soc. Entomol. Fr. 37:431-471.
36. Ohkuma M, Iida T, Kudo T. 1999. Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites.FEMS Microbiol. Lett. 181: 123-129.
37. Ohkuma M, Noda S, Kudo T. 1999. Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial communityin the gut of diverse termites. Appl. Environ. Microbiol. 65:4926-4934.
38. Ottesen EA, Leadbetter JR. 2011. Formyltetrahydrofolate synthetase gene diversity in the guts of higher termites with different diets and lifestyles. Appl. Environ. Microbiol. 77:3461-3467.
39. Pester M, Brune A. 2007. Hydrogen is the central free intermediate during lignocellulose degradation by termite gutsymbionts. ISME J. 1:551-565.
40. Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A. 2003. Axial dynamics, stability, and interspecies similarity of bacterial community structure in the highly compartmentalized gut of soil-feeding termites (Cubitermes spp.). Appl. Environ. Microbiol. 69:6018-6024.
41. Scranton MI, Novelli PC, Loud PA. 1984. The distribution and cycling of hydrogen gas in the waters of two anoxic marine environments. Limnol. Oceanogr. 29:993-1003.
42. Slaytor M. 1992. Cellulose digestion in termites and cockroaches: what role do symbionts play? Comp. Biochem. Physiol.B 103:775-784.
43. Smolenski WJ, Robinson JA. 1988. FEMS Microbiol. Lett. 53(2):95-100.
44. Tanaka H, 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.
45. Tilman D, et al. 1997. The influence of functional diversity and composition on ecosystem processes. Science 277:1300-1302.
46. Tokuda G, Watanabe H. 2007. Hidden cellulases in termites: revision of an old hypothesis. Biol. Lett. 3:336-339.
47. Warnecke F, et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560-565.
48. Wier A, et al. 2002. Spirochete and protist symbionts of a termite (Mastotermes electrodominicus) in Miocene amber.Proc. Natl. Acad. Sci. U. S. A. 99:1410-1413.
49. Wood T, Johnson R. 1986. The biology, physiology, and ecology of termites, p 1-68. In Vinson SB (ed), Economic impact and control of insects. Praeger, New York, NY.
50. Yamada A, Inoue T, Noda S, Hongoh Y, Ohkhuma M. 2007. Evolutionary trend of phylogenetic diversity of nitrogen fixation genes in the gut community of wood-feeding termites. Mol. Ecol. 16:3768-3777.
51. Yip K, et al. 2008. An integrated system for studying residue coevolution in proteins. Bioinformatics 24:290-292.