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Analysis of Termite Microbiome and Biodegradation of Various Phenolic Compounds by a Bacterium Isolated from the Termite gut in Louisiana, USA

  • Seth Van Dexter
  • Ramaraj BoopathyEmail author
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Part of the Applied Environmental Science and Engineering for a Sustainable Future book series (AESE)

Abstract

The eastern subterranean termite (EST) Reticulitermes flavipes is an insect pest in the USA. Like all wood-feeding termites (WFT), EST relies on a complex system of microbes to meet its nutritional requirements. The microbiome of WFT is stable, but the relative abundance of bacteria changes depending on diet. The purpose of this study was to explore the microbial diversity within EST collected in Thibodaux and St. Francisville, LA and detect differences based on diet and location to determine if the microbiome has a strict structure. It was found that taxa did not differ much between nearby colonies, but relative abundance is impacted by the wood in the diet. Half of bacteria from the gut of termites on nuttall oak were Bacteroidales, of which 22.7% were members of the family Porphyromonadaceae. 44% of bacteria from termites on red maple were Spirochaetes. All Spirochaetes were members of the genus Treponema. Elusimicrobia, a phylum found exclusively within termites and wood-feeding cockroaches was not abundant in either St. Francisville colony. Taxa differed more between termite colonies from different locations, but the mircobiome of St. Francisville colonies appeared to begin diverging at the family level. Overall, the microbiome was typical of termites, harboring cellulolytic protozoa, nitrogen-fixing bacteria, acetogenic Spirochaetes, and methanogenic archaeans. This has implications in microbial ecology because the organisms are changing, but the function, digestion of lignocellulose, is not. A bacterium was isolated and identified from termite gut as Acinetobacter tandoii from our previous studies degraded various phenolics, including phenol, nitrophenol, dinitrophenol, trinitrophenol, and toluene.

Keywords

Subterranean termite Microbiome Bacteroidales Spirochaetes Archaeans Phenol Nitrophenol 

References

  1. Arakawa G, Watanabe H, Yamasaki H, Maekawa H, Tokuda G (2009) Purification and molecular cloning of xylanases from the wood-feeding termite, Coptotermes formosanus Shiraki. Biosci Biotechnol Biochem 73:710–718PubMedCrossRefGoogle Scholar
  2. Beggs JD, Fewson CA (1977) Regulation and synthesis of benzyl alcohol dehydrogenase in Acinetobacter calcoaceticus NCIB8250. J Gen Microbiol 103:127–140PubMedCrossRefGoogle Scholar
  3. Boga HI, Brune A (2003) Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl Environ Microbiol 69:779–786PubMedPubMedCentralCrossRefGoogle Scholar
  4. Boopathy R (1997) Anaerobic phenol degradation by microorganisms of swine manure. Curr Microbiol 35:64–67PubMedCrossRefGoogle Scholar
  5. Boucias DG, Cai Y, Sun Y, Lietze V-U, Sen R, Raychoudhury R, Scharf ME (2013) The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its response to dietary lignocellulose composition. Mol Ecol 22:1836–1853PubMedCrossRefGoogle Scholar
  6. Brune A, Emerson D, Breznak JA (1995) The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61:2681–2687PubMedPubMedCentralCrossRefGoogle Scholar
  7. Carr EL, Kämpfer P, Patel BKC, Gürtler V, Seviour RJ (2003) Seven novel species of Acinetobacter isolated from activated sludge. Int J Syst Evol Microbiol 53:953–963PubMedCrossRefGoogle Scholar
  8. Cleveland LR (1925) The effects of oxygenation and starvation on the symbiosis between the termite, Termopsis, and its intestinal flagellates. Biol Bull., University of Chicago 48:309–326CrossRefGoogle Scholar
  9. Coy MR, Salem TZ, Denton JS, Kovaleva ES, Liu Z, Barber DS, Campbell JH, Davis DC, Buchman GW, Boucias DG, Scharf ME (2010) Phenol-oxidizing laccases from the termite gut. Insect Biochem Mol Biol 40:723–732PubMedCrossRefGoogle Scholar
  10. Desai MS, Brune A (2012) Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. 2012 The ISME Journal 6:1302–1313PubMedGoogle Scholar
  11. Dietrich C, Köhler T, Brune A (2014) The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl Environ Microbiol 80:2261–2269PubMedPubMedCentralCrossRefGoogle Scholar
  12. Doolittle M, Raina A, Lax A, Boopathy R (2007) Effect of natural products on gut microbes in Formosan subterranean termite, Coptotermes formosanus. Int Biodeterior Biodegrad 59:69–71CrossRefGoogle Scholar
  13. Doolittle M, Raina A, Lax A, Boopathy R (2008) Presence of nitrogen-fixing Klebsiella pneumoniae in the gut of the Formosan subterranean termite (Coptotermes formosanus). Bioresour Technol 99(8):3297–3300PubMedCrossRefGoogle Scholar
  14. Field JG, Clarke KR, Warwick RM (1982) A practical strategy for analysing multispecies disstribution patterns. Mar Ecol Prog Ser 8:37–52CrossRefGoogle Scholar
  15. Florane CB, Bland JM, Husseneder C, Raina AK (2004) Diet-mediated inter-colonial aggression in the Formosan subterranean termite Coptotermes formosanus. J Chem Ecol 30:2559–2574PubMedCrossRefGoogle Scholar
  16. Graber JR, Leadbetter JR, Breznak JA (2004) Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first Spirochaetes isolated from termite guts. Appl Environ Microbiol 70:1315–1320PubMedPubMedCentralCrossRefGoogle Scholar
  17. Grace JK (1997) Influence of tree extractives on foraging preferences of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 30:35–42Google Scholar
  18. Grace JK, Wood DL, Frankie GW (1989) Behavior and survival of Reticulitermes hesperus banks (Isoptera: Rhinotermitidae) on selected sawdusts and wood extracts. J Chem Ecol 15:129–139CrossRefGoogle Scholar
  19. Hongoh Y, Okhuma M, Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). FEMS Microbiol Ecol 44:231–242PubMedCrossRefPubMedCentralGoogle Scholar
  20. Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Okhuma M, Vongkaluang C, Noparatnaraporn N, Kudo T (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71:6590–6599PubMedPubMedCentralCrossRefGoogle Scholar
  21. Huang X-F, Bakker MG, Judd TM, Reardon KF, Vivanco JM (2013) Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microb Ecol 65:531–536PubMedCrossRefPubMedCentralGoogle Scholar
  22. Hungate RE (1943) Quantitative analyses on the cellulose fermentation by termite protozoa. Ann Entomol Soc Am 36:730–739CrossRefGoogle Scholar
  23. Hupert-Kocurek K, Guzik U, Wojcieszynska D (2012) Characterization of catechol 2,3-dioxygenase from Planococcus sp. strain S5 induced by high phenol concentration. Acta Biochim Pol 59:345–351PubMedCrossRefPubMedCentralGoogle Scholar
  24. Husseneder C, Berestecky JM, Grace JK (2009) Changes in composition of culturable bacterial community in the gut of the Formosan subterranean termite depending on rearing conditions of the host. Ann Entomol Soc Am 102:498–507CrossRefGoogle Scholar
  25. Husseneder C, Ho H-Y, Blackwell M (2010) Comparison of the bacterial symbiont composition of the Formosan subterranean termite from its native and introduced range. Open Microbiol J 4:53–66PubMedPubMedCentralCrossRefGoogle Scholar
  26. Jouquet P, Traoré S, Choosai C, Hartmann C, Bignell D (2011) Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur J Soil Biol 47:215–222CrossRefGoogle Scholar
  27. Ke J, Singh D, Chen S (2011) Aromatic compound degradation by the wood-feeding termite Coptotermes formosanus (Shiraki). Int Biodeterior Biodegradation 65:744–756CrossRefGoogle Scholar
  28. Kuhnigk T, Borst E-M, Ritter A, Kämpfer P, Graf A, Hertel H, König H (1994) Degradation of lignin monomers by the hindgut flora of xylophagous insects. Syst Appl Microbiol 17:76–85CrossRefGoogle Scholar
  29. Leadbetter JR, Schmidt TM, Graber JR, Breznak JA (1999) Acetogenesis from H2 plus CO2 by Spirochaetes from termite guts. Science 283:686–689PubMedCrossRefGoogle Scholar
  30. Lilburn TG, Schmidt TM, Breznak JA (1999) Phylogenetic diversity of termite gut spirochaetes. Environ Microbiol 1:331–345PubMedCrossRefGoogle Scholar
  31. Lilburn TG, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living Spirochaetes. Science 292:2495–2498PubMedCrossRefGoogle Scholar
  32. Matsuura K (2001) Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92:20–26CrossRefGoogle Scholar
  33. Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, Uchiyama H, Tanaka H (2007) Influence of feed components on symbiotic bacterial community structure in the gut of the wood-feeding higher termite Nasutitermes takasogoensis. Biosci Biotechnol Biochem 71:1244–1251PubMedCrossRefGoogle Scholar
  34. Morales-Ramos JA, Rojas MG (2001) Nutritional ecology of the Formosan subterranean termite (Isoptera: Rhinotermitidae): feeding response to commercial wood species. J Econ Entomol 94:516–523PubMedCrossRefGoogle Scholar
  35. Nalepa CA (2015) Origin of termite eusociality: trophallaxis integrates the social, nutritional, and microbial environments. Ecol Entomol 40:323–335CrossRefGoogle Scholar
  36. Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models: regression, analysis of variance, and experimental designs, 3rd edn. IRWIN, Burr Ridge, ILGoogle Scholar
  37. Noda S, Okhuma M, Yamada A, Hongoh Y, Kudo T (2003) Phylogenetic position and in situ identification of exctosymbiotic spirochaetes on protists in the termite gut. Appl Environ Microbiol 69:625–633PubMedPubMedCentralCrossRefGoogle Scholar
  38. Noda S, Hongoh Y, Sato T, Okhuma M (2009) Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites. BMC Evol Biol 9:158PubMedPubMedCentralCrossRefGoogle Scholar
  39. O’Brien RW, Breznak JA (1984) Enzymes of acetate and glucose metabolism in termites. Insect Biochem 14:639–643CrossRefGoogle Scholar
  40. Odelson DA, Breznak JA (1985) Nutrition and growth characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites. App Environ Biol 49:614–621CrossRefGoogle Scholar
  41. Okhuma M, Noda S, Kudo T (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934CrossRefGoogle Scholar
  42. Pasti MB, Pometto AL III, Nuti MP, Crawford DL (1990) Lignin-solubilizing ability of Actinomycetes isolated from termite (Termitidae) gut. Appl Environ Microbiol 56:2213–2218PubMedPubMedCentralCrossRefGoogle Scholar
  43. Potrikus CJ, Breznak JA (1981) Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. PNAS 78:4601–5605PubMedCrossRefGoogle Scholar
  44. Putrins M, Tover A, Tegova R, Saks U, Kivisaar M (2007) Study of factors which negatively affect expression of the phenol degradation operon pheBA in Pseudomonas putida. Microbiology 152:1860–1871CrossRefGoogle Scholar
  45. Rahman NA, Parks DH, Willner DL, Engelbrekston AL, Goffredi SK, Warnecke F, Scheffrahn RH, Hugenholtz P (2015) A molecular survey of Australian and north American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. Microbiome 3:5PubMedPubMedCentralCrossRefGoogle Scholar
  46. Sainsbury PD, Mineyeva Y, Mycroft Z, Bugg TD (2015) Chemical intervention in bacterial lignin degradation pathways: development of selective inhibitors for intradiol and extradiol catechol dioxygenases. Bioorg Chem 60:102–109PubMedCrossRefGoogle Scholar
  47. Scheffrahn RH, Hsu R-C, Su N-Y, Huffman JB, Midland SL, Sims JJ (1988) Allelochemical resistance of bald cypress, Taxodium distichum, heartwood to the subterranean termite, Coptotermes formosanus. J Chem Ecol 14:765–776PubMedCrossRefPubMedCentralGoogle Scholar
  48. Shen F, Lin J, Huang C (2009) Molecular detection and phylogenetic analysis of the catechol 1,2-dioxygenase gene from Gordonia spp. Syst Appl Microbiol 32:291–300PubMedCrossRefGoogle Scholar
  49. Shinzato N, Muramatsu M, Matsui T, Watanabe Y (2005) Molecular phylogenetic diversity of the bacterial community in the gut of the termite Coptotermes formosanus. Biosci Biotechnol Biochem 69:1145–1155PubMedCrossRefGoogle Scholar
  50. Smith HE, Arnott HJ (1974) Epi- and endobiotic bacteria associated with Pyrsonympha vertrens, a symbiotic protozoon of the termite Reticulitermes flavipes. Trans Am Microsc Soc 93:180–194PubMedCrossRefGoogle Scholar
  51. Stabler RM (1954) Trichomonas gallinae: a review. Exp Parasitol 3:368–402PubMedCrossRefGoogle Scholar
  52. Stanier RY, Ornston LN (1973) The Beta-ketoadipate pathway. Adv Microb Physiol 9:85–151Google Scholar
  53. Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ, Keeling PJ (2015) The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Appl Environ Microbiol 81:1059–1070PubMedPubMedCentralCrossRefGoogle Scholar
  54. Tartar A, Wheeler MM, Zhou X, Coy MR, Boucias DG, Scharf ME (2009) Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol Biofuels 2:25–29PubMedPubMedCentralCrossRefGoogle Scholar
  55. Tian M, Du D, Zhou W, Zneng X, Cheng G (2017) Phenol degradation and genotypic analysis of dioxygenase genes in bacteria isolated from sediments. Braz J Microbiol 48:305–313PubMedCrossRefGoogle Scholar
  56. Van Dexter D, Boopathy R (2018) Biodegradation of phenol by Acinetobacter tandoii isolated from the gut of the termite. Environ Sci Pollut Res 26:34067.  https://doi.org/10.1007/s11356-018-3292-4 CrossRefGoogle Scholar
  57. Van Dexter S, Boopathy R (2019) Biodegradation of phenol by Acinetobacter tandoii isolated from the gut of the termite. Environ Sci Pollut Res 26:34067–34072.CrossRefGoogle Scholar
  58. Van Dexter D, Oubre C, Boopathy R (2019) Carbon ecology of termite gut and phenol degradation by a bacterium isolated from the gut of termite. J Ind Microbiol Biotechnol 46(9–10):1265–1271. (in Print)PubMedCrossRefPubMedCentralGoogle Scholar
  59. Wang Y, Tian T, Han B, Zhao HB, Bi J, Cai B (2007) Biodegradation of phenol by free and immobilized Acinetobacter sp. strain PD12. J Environ Sci 19:222–225CrossRefGoogle Scholar
  60. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayoutte M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Otteson EA, Zhang X, Hernández M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedCrossRefPubMedCentralGoogle Scholar
  61. Watanabe Y, Shinzato N, Fukatsu T (2003) Isolation of Actinomycetes from termites’ guts. Biosci Biotechnol Biochem 67:1797–1801PubMedCrossRefPubMedCentralGoogle Scholar
  62. Wenzel M, Schönig I, Berchtold M, Kämpfer P, König H (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticolis. J Appl Microbiol 92:32–40PubMedCrossRefPubMedCentralGoogle Scholar
  63. Yamanashi T, Kim SY, Hara H, Funa N (2015) In vitro reconstitution of the catabolic reactions catalyzed by PcaHG, PcaB, and PcaL: the protocatechate branch of the β-ketoadipate pathway in Rhodococcus jostii RHA1. Biosci Biotechnol Biochem 79:830–835PubMedCrossRefPubMedCentralGoogle Scholar
  64. Yamin M (1980) Cellulose metabolism by the termite flagellate Trichomitopsis termopsidis. Appl Environ Microbiol 39:859–863PubMedPubMedCentralCrossRefGoogle Scholar
  65. Yamin MA (1981) Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria. Science 211:58–59PubMedCrossRefPubMedCentralGoogle Scholar
  66. Zhang D, Lax AR, Bland JM, Yu J, Fedorova N, Nierman WC (2010) Hydrolysis of filter-paper cellulose to glucose by two recombinant endogenous glycosyl hydrolases of Coptotermes formosanus. Insect Sci 17:245–252CrossRefGoogle Scholar
  67. Zheng H, Dietrich C, Radek R, Brune A (2016) Endomicrobium proavitum, the first isolate of Endomicrobia class. Nov. (phylum Elusimicrobia) – an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a group IV nitrogenase. Environ Microbiol 18:191–204PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biological SciencesNicholls State UniversityThibodauxUSA

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