A bacterial filter protects and structures the gut microbiome of an insect

ISME Journal

Volumn 10, Issue 8, 2016, Pages 1866-1876

  Lanan, Michele Caroline ^a   Rodrigues, Pedro Augusto Pos ^b   Agellon, Al ^b   Jansma, Patricia ^b   Wheeler, Diana Esther ^b  

^a Chr of the Natural Sciences   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANT; BACTERIUM; COMMUNITY STRUCTURE; DIGESTIVE SYSTEM; FILTER; LIFE CYCLE; MATE FIDELITY; MICROBIAL COMMUNITY; PUPATION; SYMBIONT;

SONORAN DESERT;

ANIMALIA; BACTERIA (MICROORGANISMS); CEPHALOTES; CEPHALOTES ROHWERI; FORMICIDAE; HEXAPODA; TESTUDINES;

ANIMAL; ANT; BACTERIUM; CYTOLOGY; EVOLUTION; GENETICS; INTESTINE FLORA; MICROBIOLOGY; PROVENTRICULUS;

ANIMALS; ANTS; BACTERIA; BIOLOGICAL EVOLUTION; GASTROINTESTINAL MICROBIOME; PROVENTRICULUS;

EID: 84957894957     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.264     Document Type: Article

References (52)

1. Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, Hu Y et al. (2012). Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol 21: 2282-2296
2. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. (2005). Host-bacterial mutualism in the human intestine. Science 307: 1915-1920
3. Baroni Urbani C, de Andrade ML. (1997). Pollen eating, storing, and spitting by ants. Naturwissenschaften 84: 256-258
4. Blum JE, Fischer CN, Miles J, Handelsman J. (2013). Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. mBio 4: e00860-13
5. Bové JM. (1997). Spiroplasmas: infectious agents of plants, arthropods and vertebrates. Wien Klin Wochenschr 109: 604-612
6. Bution ML, Caetano FH. (2010). The midgut of Cephalotes ants (Formicidae: Myrmicinae): ultrastructure of the epithelium and symbiotic bacteria. Micron 41: 448-454
7. Cariveau DP, Powell JE, Koch H, Winfree R, Moran NA. (2014). Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISMEJ 8: 2369-2379
8. Cassill DL, Butler J, Vinson SB, Wheeler DE. (2005). Cooperation during prey digestion between workers and larvae in the ant, Pheidole spadonia. Insect Soc 52: 339-343
9. Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD et al. (2012). Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28: 2106-2113
10. Cremer S, Sixt M. (2009). Analogies in the evolution of individual and social immunity. Philos Trans R Soc B Biol Sci 364: 129-142
11. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG et al. (2008). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8: 1-8
12. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200
13. Eisner TA. (1957). A comparative morphological study of the proventriculus of ants (Hymenoptera: Formicidae). Bull Mus Comp Zool 116: 439-490
14. Eisner TA, Wilson EO. (1952). The morphology of the proventriculus of a formicine ant. Psyche 59: 47-60
15. Engel P, Moran NA. (2013). The gut microbiota of insectsdiversity in structure and function. FEMS Microbiol Rev 37: 699-735
16. Hegedus D, Erlandson M, Gillott C, Toprak U. (2009). New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54: 285-302
17. Hölldobler B, Wilson EO. (1990). The Ants. Belknap Press of Harvard University Press: Cambridge, Massachusetts
18. Hongoh Y. (2011). Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell Mol Life Sci 68: 1311-1325
19. Hu Y, Lukasik P, Moreau CS, Russell JA. (2014). Correlates of gut community composition across an ant species (Cephalotes varians) elucidate causes and consequences of symbiotic variability. Mol Ecol 23: 1284-1300
20. Jarvis JU. (1981). Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212: 571-573
21. Jones RT, Vetter SM, Montenieiri J, Holmes J, Bernhardt SA, Gage KL. (2013). Yersinia pestis infection and laboratory conditions alter flea-associated bacterial communities. ISMEJ 7: 224-228
22. Kautz S, Rubin BE, Moreau CS. (2013). Bacterial infections across the ants: frequency and prevalence of Wolbachia, Spiroplasma, and Asaia. Psyche 2013: 1-12
23. Koch H, Schmid-Hempel P. (2011). Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 108: 19288-19292
24. Kohler 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
25. Kwong WK, Moran NA. (2015). Evolution of host specialization in gut microbes: the bee gut as a model. Gut Microbes 6: 214-220
26. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T, Douglas AE et al. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110: 3229-3236
27. Moran NA, Mccutcheon JP, Nakabachi A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190
28. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970-974
29. Nelson AM, Walk ST, Taube S, Taniuchi M, Houpt ER, Wobus CE et al. (2012). Disruption of the human gut microbiota following Norovirus infection. PLoS One 7: e48224
30. Neuwirth E. (2014). RColorBrewer: ColorBrewer Palettes. R package version 1.1-2 Available at: http://CRAN.Rproject. org/package = RColorBrewer
31. Nyholm SV, McFall-Ngai M. (2004). The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2: 632-642
32. Nyholm SV, Graf J. (2012). Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nat Rev Microbiol 10: 815-827
33. Ohbayashi T, Takeshita K, Kitagawa W, Nikoh N, Koga R, Meng XY et al. (2015). Insect's intestinal organ for symbiont sorting. Proc Natl Acad Sci USA 112: E5179-E5188
34. Oksanen J et al. (2015). Vegan: Community Ecology Package. R package version 2.3-0 Available at: http:// CRAN.R-project.org/package = vegan
35. Paradis E, Claude J, Strimmer K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290
36. Pernice M, Simpson SJ, Ponton F. (2014). Towards an integrated understanding of gut microbiota using insects as model systems. J Insect Physiol 69: 12-18
37. Powell S. (2008). Ecological specialization and evolution of a specialized caste in Cephalotes ants. Funct Ecol 22: 902-911
38. 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
39. Razin S, Hayflick L. (2010). Highlights of mycoplasma research-an historal perspective. Biologicals 38: 183-190
40. Razin S, Yogev D, Naot Y. (1998). Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev 62: 1094-1156
41. Roche RK, Wheeler DE. (1997). Morphological specializations of the digestive tract of Zacryptocerus rohweri (Hymenoptera: Formicidae). J Morphol 234: 253-262
42. Russell J, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106: 21236-21241
43. Sanders JG, Powell S, Kronauer DJ, Vasconcelos HL, Frederickson ME, Pierce NE. (2014). Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol 23: 1268-1283
44. Sansonetti PJ. (2004). War and peace at mucosal surfaces. Nat Rev Immunol 4: 953-964
45. Schloss PD. (2009). A high-throughput DNA sequence aligner for microbial ecology studies. PLoS One 14: e8230
46. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: open-source, platform-independent, communitysupported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541
47. Stecher B, Maier L, Hardt WD. (2013). 'Blooming' in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11: 277-284
48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729
49. Team RDC. (2008). R: A language and environment for statistical computing. In: Computing RFFS. (ed.). Vienna, Austria. Available at: http://www.R-project.org
50. Wheeler DE. (1984). Behavior of the ant, Procryptocerus scabriusculus (Hymenoptera: Formicidae), with comparisons to other Cephalotines. Psyche 91: 171-192
51. Wilson EO. (1976). A social ethogram of the neotropical arboreal ant Zacryptocerus varians (Fr. Smith). Anim Behav 24: 354-363
52. Yanoviak SP, Kaspari M, Dudley R, Poinar G. (2008). Parasite-induced fruit mimicry in a tropical canopy ant. Am Nat 171: 536-544