Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis

Applied and Environmental Microbiology

Volumn 78, Issue 1, 2012, Pages 204-210

  Sabree, Zakee L ^a   Huang, Charlie Ye ^a   Arakawa, Gaku ^b   Tokuda, Gaku ^c   Lo, Nathan ^d   Watanabe, Hirofumi ^b   Moran, Nancy A ^a  

^a YALE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF THE RYUKYUS   (Japan)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOSYMBIONT; ESSENTIAL AMINO ACIDS; GUT MICROBES; MICROBIAL ASSEMBLAGE; MICROBIOTAS; SOCIAL BEHAVIOR; TERMITE GUT;

AMINO ACIDS; BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; GENES; NITROGEN FIXATION;

NUTRIENTS;

BACTERIAL DNA;

AMINO ACID; BACTERIUM; COCKROACH; DIET; DIVERGENCE; ENDOSYMBIONT; GENOME; LIGNIN; MICROBIAL COMMUNITY; NUTRIENT; SOCIAL BEHAVIOR; TERMITE; VITAMIN;

ANIMAL; ARTICLE; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; COMPARATIVE STUDY; DNA SEQUENCE; FLAVOBACTERIACEAE; GENETIC SELECTION; GENETICS; GENOME SIZE; ISOPTERA; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; BACTERIAL PHYSIOLOGICAL PHENOMENA; BASE SEQUENCE; DNA, BACTERIAL; FLAVOBACTERIACEAE; GENOME SIZE; GENOME, BACTERIAL; ISOPTERA; METAGENOME; MOLECULAR SEQUENCE DATA; PHYLOGENY; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

BLATTABACTERIUM; BLATTARIA; HEXAPODA; ISOPTERA; MASTOTERMES DARWINIENSIS;

EID: 84862932996     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06540-11     Document Type: Article

References (82)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104-2105.
2. Akman L, et al. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32: 402-407.
3. Baba T, et al. 2006. Construction of Escherichia coli K-12 in-frame, singlegene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
4. Bandi C, et al. 1995. The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc. Biol. Sci. 259:293-299.
5. Bandi C, Siron M, Nalepa CA, Corona S, Sacchi L. 1997. Phylogenetically distant intracellular symbionts in termites. Parassitologia 39:71-75.
6. Bandi C, Sacchi L. 2000. Intracellular symbiosis in termites, p 261-273. In Abe T, Bignell DE, and Higashi M (ed), Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publisher, Dordrecht, The Netherlands.
7. Bell WJ, Roth LM, Nalepa CA. 2007. Cockroaches: ecology, behavior, and natural history, p 150-164. Johns Hopkins University Press, Baltimore, MD.
8. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2011. GenBank. Nucleic Acids Res. 39:D32-D37.
9. Bourtzis K, Miller TA. 2006. Insect symbiosis. CRC Press, Taylor & Francis Group Boca Raton, FL.
10. Brugerolle G. 2004. Devescovinid features, a remarkable surface cytoskeleton, and epibiotic bacteria revisited in Mixotricha paradoxa, a parabasalid flagellate. Protoplasma 224:49-59.
11. N) transcription factor. J. Bacteriol. 182:4129-4136.
12. Camacho C, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421.
13. 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.
14. Courrent A, et al. 2008. The fine structure of colleterial glands in two cockroaches and three termites, including a detailed study of Cryptocercus punctulatus (Blattaria, Cryptocercidae) and Mastotermes darwiniensis (Isoptera, Mastotermitidae). Arthropod Struct. Dev. 37:55-66.
15. Cruden DL, Markovetz AJ. 1984. Microbial aspects of the cockroach hindgut. Arch. Microbiol. 138:131-139.
16. Degnan PH, Lazarus AB, Wernegreen JJ. 2005. Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res. 15:1023-1033.
17. Droge S, Frohlich J, Radek R, Konig H. 2006. Spirochaeta coccoides sp. nov., a novel coccoid spirochete from the hindgut of the termite Neotermes castaneus. Appl. Environ. Microbiol. 72:392-397.
18. Droge S, Rachel R, Radek R, Konig H. 2008. Treponema isoptericolens sp. nov., a novel spirochaete from the hindgut of the termite Incisitermes tabogae. Int. J. Syst. Evol. Microbiol. 58:1079-1083.
19. Emerson A. 1965. A review of the Mastotermitidae (Isoptera), including a new fossil genus from Brazil. Am. Mus. Novitates 2236:1-46.
20. Finn RD, et al. 2010. The pfam protein families database. Nucleic Acids Res. 38:D211-D222.
21. Fukatsu T, Ishikawa H. 1996. Phylogenetic position of yeast-like symbiont of Hamiltonaphis styraci (Homoptera, Aphididae) based on 18S rDNA sequence. Insect Biochem. Mol. Biol. 26:383-388.
22. Gerdes SY, et al. 2002. From genetic footprinting to antimicrobial drug targets: examples in cofactor biosynthetic pathways. J. Bacteriol. 184: 4555-4572.
23. Guindon S, et al. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321.
24. Hackstein JHP, Stumm CK. 1994. Methane production in terrestrial arthropods. Proc. Natl. Acad. Sci. U. S. A. 91:5441-5445.
25. Hongoh Y, Ohkuma M, Kudo T. 2003. Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol. Ecol. 44:231-242.
26. 2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108-1109.
27. Hoyte HMD. 1961. The protozoa occurring in the hind-gut of cockroaches. 2. Morphology of Nyctotherus ovalis. Parasitology 51:437-463.
28. Hyatt D, et al. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119.
29. Inward D, Beccaloni G, Eggleton P. 2007. Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Lett. 3:331-335.
30. Kambhampati S, Kjer KM, Thorne BL. 1996. Phylogenetic relationship among termite families based on DNA sequence of mitochondrial 16S ribosomal RNA gene. Insect Mol. Biol. 5:229-238.
31. Katoh K, Asimenos G, Toh H. 2009. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537:39-64.
32. Kuriwada T, et al. 2010. Biological role of Nardonella endosymbiont in its weevil host. PLoS One 5:e13101.
33. Kurtz S, et al. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12.
34. Laslett D, Canback B, Andersson S. 2002. BRUCE: a program for the detection of transfer-messenger RNA genes in nucleotide sequences. Nucleic Acids Res. 30:3449-3453.
35. Lefevre C, et al. 2004. Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial replacement. Mol. Biol. Evol. 21:965-973.
36. Lerat E, Daubin V, Moran NA. 2003. From gene trees to organismal phylogeny in prokaryotes: the case of the γ-Proteobacteria. PLoS Biol. 1:E19.
37. Lo N, et al. 2000. Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr. Biol. 10:801-804.
38. 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.
39. Lopez-Sanchez MJ, et al. 2009. Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet. 5:e1000721.
40. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
41. Machida M, Kitade O, Miura T, Matsumoto T. 2001. Nitrogen recycling through proctodeal trophallaxis in the Japanese damp-wood termite Hodotermopsis japonica (Isoptera, Termopsidae). Insectes Soc. 48:52-56.
42. Maekawa K, Kon M, Matsumoto T, Araya K, Lo N. 2005. Phylogenetic analyses of fat body endosymbionts reveal differences in invasion times of blaberid wood-feeding cockroaches (Blaberidae: Panesthiinae) into the Japanese archipelago. Zool. Sci. 22:1061-1067.
43. Mazel D, Pochet S, Marliere P. 1994. Genetic characterization of polypeptide deformylase, a distinctive enzyme of eubacterial translation. EMBO J. 13:914-923.
44. McCutcheon JP, Moran NA. 2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. U. S. A. 104:19392-19397.
45. McCutcheon JP, McDonald BR, Moran NA. 2009. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet. 5:e1000565.
46. McCutcheon JP, McDonald BR, Moran NA. 2009. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. U. S. A. 106:15394-15399.
47. McCutcheon JP, Moran NA. 2010. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2:708-718.
48. Moran NA. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. U. S. A. 93:2873-2878.
49. Moran NA, Tran P, Gerardo NM. 2005. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Environ. Microbiol. 71:8802-8810.
50. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165-190.
51. Nakabachi A, et al. 2006. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267.
52. Nakajima H, Hongoh Y, Usami R, Kudo T, Ohkuma M. 2005. Spatial distribution of bacterial phylotypes in the gut of the termite Reticulitermes speratus and the bacterial community colonizing the gut epithelium. FEMS Microbiol. Ecol. 54:247-255.
53. Nakajima H, et al. 2006. Phylogenetic and morphological diversity of Bacteroidales members associated with the gut wall of termites. Biosci. Biotechnol. Biochem. 70:211-218.
54. Nakashima KI, Watanabe H, Azuma JI. 2002. Cellulase genes from the parabasalian symbiont Pseudotrichonympha grassii in the hindgut of the wood-feeding termite Coptotermes formosanus. Cell. Mol. Life Sci. 59: 1554-1560.
55. Nalepa CA, Lenz M. 2000. The ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae. Proc. Biol. Sci. 267:1809-1813.
56. Nalepa CA, Bignell DE, Bandi C. 2001. Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insectes Soc. 48: 194-201.
57. Noda S, et al. 2007. Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol. Ecol. 16:1257-1266.
58. Ohkuma M, Noda S, Hongoh Y, Nalepa CA, Inoue T. 2009. Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc. Biol. Sci. 276:239-245.
59. Ohtoko K, et al. 2000. Diverse genes of cellulase homologues of glycosyl hydrolase family 45 from the symbiotic protists in the hindgut of the termite Reticulitermes speratus. Extremophiles 4:343-349.
60. Poinar, GO, Jr. 2009. Description of an early cretaceous termite (Isoptera: Kalotermitidae) and its associated intestinal protozoa, with comments on their co-evolution. Parasit. Vectors 2:12.
61. Potrikus CJ, Breznak JA. 1980. Uric acid-degrading bacteria in guts of termites [Reticulitermes flavipes (Kollar)]. Appl. Environ. Microbiol. 40: 117-124.
62. Potrikus CJ, Breznak JA. 1981. Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. Proc. Natl. Acad. Sci. U. S. A. 78:4601-4605.
63. Pruesse E, 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.
64. Radek R, Nitsch G. 2007. Ectobiotic spirochetes of flagellates from the termite Mastotermes darwiniensis: attachment and cyst formation. Eur. J. Protistol. 43:281-294.
65. Sabree ZL, Kambhampati S, Moran NA. 2009. Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc. Natl. Acad. Sci. U. S. A. 106:19521-19526.
66. Sabree ZL, Degnan PH, Moran NA. 2010. Chromosome stability and gene loss in cockroach endosymbionts. Appl. Environ. Microbiol. 76: 4076-4079.
67. Sacchi L, et al. 1998. Some aspects of intracellular symbiosis during embryo development of Mastotermes darwiniensis (Isoptera: Mastotermitidae). Parassitologia 40:309-316.
68. Sacchi L, et al. 2000. Transovarial transmission of symbiotic bacteria in Mastotermes darwiniensis (Isoptera: Mastotermitidae): ultrastructural aspects and phylogenetic implications. Ann. Entomol. Soc. Am. 93: 1308-1313.
69. Schloss PD, et al. 2009. Introducing mothur: open-source, platformindependent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
70. Selengut JD, et al. 2007. TIGRFAMs and genome properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res. 35:D260-D264.
71. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86.
72. Stancek M, Schnell R, Ryden-Aulin M. 2005. Analysis of Escherichia coli nicotinate mononucleotide adenylyltransferase mutants in vivo and in vitro. BMC Biochem. 6:16.
73. Tamas I, et al. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.
74. Tamas I, et al. 2008. Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proc. Natl. Acad. Sci. U. S. A. 105:14934-14939.
75. Tatusov RL, et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41.
76. van Ham RC, et al. 2003. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. U. S. A. 100:581-586.
77. van Hijum SA, Zomer AL, Kuipers OP, Kok J. 2005. Projector 2: contig mapping for efficient gap-closure of prokaryotic genome sequence assemblies. Nucleic Acids Res. 33:W560-W566.
78. Warnecke F., et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560-565.
79. Wenzel M, Schonig I, Berchtold M, Kampfer P, Konig H. 2002. Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J. Appl. Microbiol. 92:32-40.
80. Wenzel M, Radek R, Brugerolle G, Konig H. 2003. Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur. J. Protistol. 39:11-23.
81. Wu D, et al. 2006. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4:e188.
82. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821-829.