Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments

ISME Journal

Volumn 10, Issue 8, 2016, Pages 1998-2009

  Berg, Maureen ^a   Stenuit, Ben ^b   Ho, Joshua ^a   Wang, Andrew ^a   Parke, Caitlin ^a   Knight, Matthew ^a   Alvarez Cohen, Lisa ^b   Shapira, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b 109 McLaughlin Hall   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPARATIVE STUDY; EXPERIMENTAL STUDY; GENETIC ANALYSIS; GENETIC VARIATION; HOMOGENEITY; HOST USE; LABORATORY METHOD; MICROBIAL COMMUNITY; NEMATODE; NICHE; SOIL MICROORGANISM;

CAENORHABDITIS ELEGANS; VERTEBRATA;

SOIL;

ANIMAL; CAENORHABDITIS ELEGANS; DIET; DNA SEQUENCE; ENVIRONMENT; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; INTESTINE; INTESTINE FLORA; MICROBIOLOGY; POPULATION GENETICS; SOIL;

ANIMALS; CAENORHABDITIS ELEGANS; DIET; ENVIRONMENT; GASTROINTESTINAL MICROBIOME; GENETIC VARIATION; GENETICS, POPULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INTESTINES; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY;

EID: 84955326227     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.253     Document Type: Article

References (71)

1. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR et al. (2011). Enterotypes of the human gut microbiome. Nature 473: 174-180
2. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y et al. (2011). Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-341
3. Avery L, Shtonda BB. (2003). Food transport in the C. elegans pharynx. J Exp Biol 206: 2441-2457
4. Barriere A, Felix MA. (2014). Isolation of C. elegans and related nematodes. WormBook 2: 1-19
5. Bartlett JG. (2002). Clinical practice. Antibiotic-associated diarrhea. N Engl J Med 346: 334-339
6. Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE, Guillemin K. (2006). Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297: 374-386
7. Caceres MD, Legendre P. (2009). Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566-3574
8. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336
9. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al. (2012). Ultra-highthroughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621-1624
10. Cariveau DP, Elijah Powell J, Koch H, Winfree R, Moran NA. (2014). Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J 8: 2369-2379
11. Carmody RN, Gerber GK, Luevano JM Jr., Gatti DM, Somes L, Svenson KL et al. (2015). Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17: 72-84
12. Chaston JM, Newell PD, Douglas AE. (2014). Metagenomewide association of microbial determinants of host phenotype in Drosophila melanogaster. MBio 5: e01631-01614
13. Choi JI, Yoon KH, Subbammal Kalichamy S, Yoon SS, Il Lee J. (2016). A natural odor attraction between lactic acid bacteria and the nematode Caenorhabditis elegans. ISME J 10: 558-567
14. Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB et al. (2012). Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149: 1578-1593
15. Clemente JC, Ursell LK, Parfrey LW, Knight R. (2012). The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270
16. Compant S, Nowak J, Coenye T, Clement C, Ait Barka E. (2008). Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32: 607-626
17. Consortium HMP (2012). Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214
18. Coolon JD, Jones KL, Todd TC, Carr BC, Herman MA. (2009). Caenorhabditis elegans genomic response to soil bacteria predicts environment-specific genetic effects on life history traits. PLoS Genet 5: e1000503
19. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. (2012). The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255-1262
20. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559-563
21. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S et al. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107: 14691-14696
22. de Hoon MJ, Imoto S, Nolan J, Miyano S. (2004). Open source clustering software. Bioinformatics 20: 1453-1454
23. Delgado S, Cabrera-Rubio R, Fau-Mira A, Mira A, Fau-Suarez A, Suarez A et al. (2013). Microbiological survey of the human gastric ecosystem using culturing and pyrosequencing methods. Microb Ecol 65 (3): 763-772
24. Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, Dinkelacker I et al. (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 40: 1193-1198
25. Dishaw LJ, Flores-Torres J, Lax S, Gemayel K, Leigh B, Melillo D et al. (2014). The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS One 9: e93386
26. Dormann CF, Gruber B, Dormann MCF, Depends M. (2008). The Bipartite Package Version 073 R project for Statistical Computing: Vienna, Austria
27. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461
28. Eisen MB, Spellman PT, Brown PO, Botstein D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868
29. Erkosar B, Leulier F. (2014). Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model. FEBS Lett 588: 4250-4257
30. Faith DP. (1994). Phylogenetic pattern and the quantification of organismal biodiversity. Philos Trans R Soc Lond Ser B 345: 45-58
31. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J et al. (2012). Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8: e1002606
32. Felix MA, Jovelin R, Ferrari C, Han S, Cho YR, Andersen EC et al. (2013). Species richness, distribution and genetic diversity of Caenorhabditis nematodes in a remote tropical rainforest. BMC Evol Biol 13: 10
33. Franz CJ, Renshaw H, Frezal L, Jiang Y, Felix MA, Wang D. (2014). Orsay, Santeuil and Le Blanc viruses primarily infect intestinal cells in Caenorhabditis nematodes. Virology 448: 255-264
34. Gihring TM, Green SJ, Schadt CW. (2012). Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environ Microbiol 14: 285-290
35. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R et al. (2014). Human genetics shape the gut microbiome. Cell 159: 789-799
36. Grewal PS. (1991). Influence of bacteria and temperature on the reproduction of Caenorhabditis elegans (Nematoda: Rhabditidae) infesting mushrooms (Agaricus bisporus). Nematologica 37: 72-82
37. Gusarov I, Gautier L, Smolentseva O, Shamovsky I, Eremina S, Mironov A et al. (2013). Bacterial nitric oxide extends the lifespan of C. elegans. Cell 152: 818-830
38. Hamady M, Knight R. (2009). Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 19: 1141-1152
39. Hodgkin J, Felix MA, Clark LC, Stroud D, Gravato-NobreMJ. (2013). Two Leucobacter strains exert complementary virulence on Caenorhabditis including death by wormstar formation. Curr Biol 23: 2157-2161
40. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U et al. (2009). Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498
41. Kiontke KC, Felix MA, Ailion M, Rockman MV, Braendle C, Penigault JB et al. (2011). A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol 11: 339
42. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R et al. (2011). Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108(Suppl 1): 4578-4585
43. Ladygina N, Johansson T, Canback B, Tunlid A, Hedlund K. (2009). Diversity of bacteria associated with grassland soil nematodes of different feeding groups. FEMS Microbiol Ecol 69: 53-61
44. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. (2005). Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070-11075
45. Lozupone C, Knight R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235
46. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC et al. (2007). Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2: 204
47. MacNeil LT, Watson E, Arda HE, Zhu LJ, Walhout AJ. (2013). Diet-induced developmental acceleration independent of TOR and insulin in C. elegans. Cell 153: 240-252
48. McDonald KL, Webb RI. (2011). Freeze substitution in 3 hours or less. J Microsc 243: 227-233
49. McKnite AM, Perez-Munoz ME, Lu L, Williams EG, Brewer S, Andreux PA et al. (2012). Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PLoS One 7: e39191
50. McMurdie PJ, Holmes S. (2013). Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8: e61217
51. Montalvo-Katz S, Huang H, Appel MD, Berg M, Shapira M. (2013). Association with soil bacteria enhances p38-dependent infection resistance in Caenorhabditis elegans. Infect Immun 81: 514-520
52. Otani S, Mikaelyan A, Nobre T, Hansen LH, Kone NA, Sorensen SJ et al. (2014). Identifying the core microbial community in the gut of fungus-growing termites. Mol Ecol 23: 4631-4644
53. Petersen C, Dirksen P, Schulenburg H. (2015). Why we need more ecology for genetic models such as C. elegans. Trends Genet 31: 120-127
54. Rae R, Riebesell M, Dinkelacker I, Wang Q, Herrmann M, Weller AM et al. (2008). Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences. J Exp Biol 211: 1927-1936
55. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB et al. (2009). The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7: 514-525
56. Shannon CE. (1997). The mathematical theory of communication. 1963. MD Comput 14: 306-317
57. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504
58. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. (2011). Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35: 652-680
59. Sivasundar A, Hey J. (2005). Sampling from natural populations with RNAI reveals high outcrossing and population structure in Caenorhabditis elegans. Curr Biol 15: 1598-1602
60. Staib L, Fuchs TM. (2014). From food to cell: nutrient exploitation strategies of enteropathogens. Microbiology 160: 1020-1039
61. Stone L, Roberts A. (1990). The checkerboard score and species distributions. Oecologia 85: 74-79
62. Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, Kleerebezem M et al. (2013). Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J 7: 707-717
63. Tokuda G, Watanabe H. (2007). Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3: 336-339
64. Tremblay J, Singh K, Fern A, Barriere A, Kirton ES, He S, Woyke T et al. (2015). Primer and platform effects on 16S rRNA tag sequencing. Front Microbiol 6: 771
65. Troemel ER, Felix MA, Whiteman NK, Barriere A, Ausubel FM. (2008). Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 6: 2736-2752
66. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031
67. Vojvodic S, Rehan SM, Anderson KE. (2013). Microbial gut diversity of Africanized and European honey bee larval instars. PLoS One 8: e72106
68. Wong AC, Chaston JM, Douglas AE. (2013). The inconstant gut microbiota of Drosophila species revealed by 16 S rRNA gene analysis. ISME J 7: 1922-1932
69. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108
70. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC et al. (2003). A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299: 2074-2076
71. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M et al. (2012). Human gut microbiome viewed across age and geography. Nature 486: 222-227