Host genotype and microbiota contribute asymmetrically to transcriptional variation in the threespine stickleback gut

Genome Biology and Evolution

Volumn 9, Issue 3, 2017, Pages 504-520

  Small, Clayton M ^a   Milligan Myhre, Kathryn ^a,b   Bassham, Susan ^a   Guillemin, Karen ^a   Cresko, William A ^a  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF ALASKA ANCHORAGE   (United States)

Author keywords

Fish model; Genotype by environment interaction; Gnotobiology; Host microbe systems; RNA seq

Indexed keywords

RNA 16S;

ANIMAL; GENETIC TRANSCRIPTION; GENETICS; GENOTYPE; INNATE IMMUNITY; MICROBIOLOGY; MICROFLORA; MOLECULAR EVOLUTION; SMEGMAMORPHA;

ANIMALS; EVOLUTION, MOLECULAR; GENOTYPE; IMMUNITY, INNATE; MICROBIOTA; RNA, RIBOSOMAL, 16S; SMEGMAMORPHA; TRANSCRIPTION, GENETIC;

EID: 85032157815     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evx014     Document Type: Article

References (91)

1. Albert FW, Kruglyak L. 2015. The role of regulatory variation in complex traits and disease. Nat Rev Genet. 16:197-212.
2. Albertson RC, Cresko W, Detrich HW, 3rd, Postlethwait JH. 2009. Evolutionary mutant models for human disease. Trends Genet. 25:74-81.
3. Backhed F, et al. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 101:15718-15723.
4. Bates JM, et al. 2006. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol. 297:374-386.
5. Bell MA, Foster SA. 1994. The evolutionary biology of the threespine stickleback. Oxford: University Press.
6. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B-Methodol. 57:289-300.
7. Benson AK, et al. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A. 107:18933-18938.
8. Broderick NA, Buchon N, Lemaitre B. 2014. Microbiota-induced changes in drosophila melanogaster host gene expression and gut morphology. MBio 5:e01117-e01114.
9. Burns AR, et al. 2016. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 10:655-664.
10. Camp JG, et al. 2014. Microbiota modulate transcription in the intestinal epithelium without remodeling the accessible chromatin landscape. Genome Res. 24:1504-1516.
11. Carlson M. 2016. org.Hs.eg.db: Genome wide annotation for Human. R package version 3.2.3.
12. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA. 2013. Stacks: an analysis tool set for population genomics. Mol Ecol. 22:3124-3140.
13. Civelek M, Lusis AJ. 2014. Systems genetics approaches to understand complex traits. Nat Rev Genet. 15:34-48.
14. Colosimo PF, et al. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2:E109.
15. Coolon JD, McManus CJ, Stevenson KR, Graveley BR, Wittkopp PJ. 2014. Tempo and mode of regulatory evolution in Drosophila. Genome Res. 24:797-808.
16. Coutermarsh-Ott S, Eden K, Allen IC. 2016. Beyond the inflammasome: regulatory NOD-like receptor modulation of the host immune response following virus exposure. J Gen Virol. 97:825-838.
17. Cresko WA, et al. 2004. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci U S A. 101:6050-6055.
18. Davenport ER, et al. 2015. Genome-wide association studies of the human gut microbiota. PLoS One 10:e0140301.
19. Dethlefsen L, McFall-Ngai M, Relman DA. 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811-818.
20. Falcon S, Gentleman R. 2007. Using GOstats to test gene lists for GO term association. Bioinformatics 23:257-258.
21. Gillilland MG, 3rd, et al. 2012. Ecological succession of bacterial communities during conventionalization of germ-free mice. Appl Environ Microbiol. 78:2359-2366.
22. Glazer AM, Killingbeck EE, Mitros T, Rokhsar DS, Miller CT. 2015. Genome assembly improvement and mapping convergently evolved skeletal traits in sticklebacks with genotyping-by-sequencing. G3 (Bethesda) 5:1463-1472.
23. Good SR, et al. 2009. Temporal induction pattern of STAT4 target genes defines potential for Th1 lineage-specific programming. J Immunol. 183:3839-3847.
24. Goodrich JK, et al. 2014. Human genetics shape the gut microbiome. Cell 159:789-799.
25. Goodrich JK, Davenport ER, Waters JL, Clark AG, Ley RE. 2016. Cross-species comparisons of host genetic associations with the microbiome. Science 352:532-535.
26. Griffiths R. 2000. DNA sex identification in the three-spined stickleback. J Fish Biol. 57:1331-1334.
27. Gultekin Y, Eren E, Ozoren N. 2015. Overexpressed NLRC3 acts as an anti-inflammatory cytosolic protein. J Innate Immun. 7:25-36.
28. Hildebrand F, et al. 2013. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 14:R4.
29. Hodgins-Davis A, Townsend JP. 2009. Evolving gene expression: from G to E to GxE. Trends Ecol Evol. 24:649-658.
30. Hohenlohe PA, et al. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6:e1000862.
31. Hooper LV, et al. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881-884.
32. Huang Y, et al. 2016. Transcriptome profiling of immune tissues reveals habitat-specific gene expression between lake and river sticklebacks. Mol Ecol. 25:943-958.
33. Huber S, et al. 2012. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491:259-263.
34. Huttenhower C, Kostic AD, Xavier RJ. 2014. Inflammatory bowel disease as a model for translating the microbiome. Immunity 40:843-854.
35. Hutter S, Saminadin-Peter SS, Stephan W, Parsch J. 2008. Gene expression variation in African and European populations of Drosophila melanogaster. Genome Biol. 9:R12.
36. Jabeen R, et al. 2015. Altered STAT4 Isoform Expression in Patients with Inflammatory Bowel Disease. Inflamm Bowel Dis 21:2383-2392.
37. Kanther M, et al. 2011. Microbial colonization induces dynamic temporal and spatial patterns of NF-kappaB activation in the zebrafish digestive tract. Gastroenterology 141:197-207.
38. Kanther M, et al. 2014. Commensal microbiota stimulate systemic neutrophil migration through induction of serum amyloid A. Cell Microbiol. 16:1053-1067.
39. Kimmel CB, et al. 2005. Evolution and development of facial bone morphology in threespine sticklebacks. Proc Natl Acad Sci U S A. 102:5791-5796.
40. Kimmel CB, Hohenlohe PA, Ullmann B, Currey M, Cresko WA. 2012. Developmental dissociation in morphological evolution of the stickleback opercle. Evol Dev. 14:326-337.
41. Ko DC, et al. 2009. A genome-wide in vitro bacterial-infection screen reveals human variation in the host response associated with inflammatory disease. Am J Hum Genet. 85:214-227.
42. Kubinak JL, et al. 2015. MyD88 signaling in T cells directs IgA-mediated control of the microbiota to promote health. Cell Host Microb. 17:153-163.
43. Lam SH, Chua HL, Gong Z, Lam TJ, Sin YM. 2004. Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Develop Comp Immunol 28:9-28.
44. Law CW, Chen Y, Shi W, Smyth GK. 2014. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15:R29.
45. Leamy LJ, et al. 2014. Host genetics and diet, but not immunoglobulin A expression, converge to shape compositional features of the gut microbiome in an advanced intercross population of mice. Genome Biol. 15:552.
46. Leder EH, et al. 2010. Female-biased expression on the X chromosome as a key step in chromosome evolution in threespine sticklebacks. Mol Biol Evol. 27:1495-1503.
47. Leder EH, et al. 2015. The evolution and adaptive potential of transcriptional variation in sticklebacks-signatures of selection and widespread heritability. Mol Biol Evol. 32:674-689.
48. Lenz TL, Eizaguirre C, Rotter B, Kalbe M, Milinski M. 2013. Exploring local immunological adaptation of two stickleback ecotypes by experimental infection and transcriptome-wide digital gene expression analysis. Mol Ecol. 22:774-786.
49. Leung Y, Dowling J. 2005. Gene expression profiling of zebrafish embryonic retina. Zebrafish 2:269.
50. Levy M, Thaiss CA, Katz MN, Suez J, Elinav E. 2015. Inflammasomes and the microbiota-partners in the preservation of mucosal homeostasis. Semin Immunopathol 37:39-46.
51. Levy M, et al. 2015. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163:1428-1443.
52. Luo W, Brouwer C. 2013. Pathview: an R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics 29:1830-1831.
53. Luo W, Friedman MS, Shedden K, Hankenson KD, Woolf PJ. 2009. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 10:161.
54. Lupu F, Keshari RS, Lambris JD, Coggeshall KM. 2014. Crosstalk between the coagulation and complement systems in sepsis. Thromb Res. 133(Suppl 1):S28-S31.
55. Mai V, Prosperi M, Yaghjyan L. 2016. Moving microbiota research toward establishing causal associations that represent viable targets for effective public health interventions. Ann Epidemiol. 26:306-310.
56. McCafferty J, et al. 2013. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. ISME J. 7:2116-2125.
57. McFall-Ngai M, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A. 110:3229-3236.
58. McKnite AM, et al. 2012. Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PLoS One 7:e39191.
59. Milligan-Myhre K, et al. 2016. Innate immune responses to gut microbiota differ between oceanic and freshwater threespine stickleback populations. Dis Model Mech. 9:187-198.
60. Morgan XC, et al. (Morgan2015 co-authors). 2015. Associations between host gene expression, the mucosal microbiome, and clinical outcome in the pelvic pouch of patients with inflammatory bowel disease. Genome Biol. 16:1-15.
61. Morgan M, Falcon S, Gentleman R. 2016. GSEABase: gene set enrichment data structures and methods. R package version 1.34.1.
62. Nguyen KB, et al. 2002. Critical role for STAT4 activation by type 1 inter-ferons in the interferon-gamma response to viral infection. Science 297:2063-2066.
63. Nikinmaa M, et al. 2013. Transcription and redox enzyme activities: comparison of equilibrium and disequilibrium levels in the three-spined stickleback. Proc R Soc B. 280:20122974.
64. Nolte AW, Renaut S, Bernatchez L. 2009. Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation. BMC Evol Biol. 9:59.
65. Oksanen J, et al. 2016. vegan: Community Ecology Package. R package version 2.3-5.
66. Opipari A, Franchi L. 2015. Role of inflammasomes in intestinal inflammation and Crohn's disease. Inflamm Bowel Dis. 21:173-181.
67. Org E, et al. 2015. Genetic and environmental control of host-gut microbiota interactions. Genome Res. 25:1558-1569.
68. Orozco LD, et al. 2012. Unraveling inflammatory responses using systems genetics and gene-environment interactions in macrophages. Cell 151:658-670.
69. Pages H, Carlson M, Falcon S, Li N. 2016. AnnotationDbi: Annotation Database Interface. R package version 1.34.4.
70. Park MC, Lee SW, Park YB, Lee SK. 2015. AB0128 expression patterns of nod-like receptors in rheumatoid synovium and its effect on inflammatory responses of rheumatoid fibroblast-like synoviocytes. Ann Rheumat Dise. 74:933.932-933.
71. Peichel CL, et al. 2004. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol. 14:1416-1424.
72. Poelstra JW, et al. 2014. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344:1410-1414.
73. Quach H, et al. 2016. Genetic adaptation and neandertal admixture shaped the immune system of human populations. Cell 167:643-656 e617.
74. R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
75. Rawls JF, Samuel BS, Gordon JI. 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci U S A. 101:4596-4601.
76. Richards AL, et al. 2016. Genetic and transcriptional analysis of human host response to healthy gut microbiota. mSystems. 1:
77. Ritchie ME, et al. 2015. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43:e47.
78. Rittirsch D, Flierl MA, Ward PA. 2008. Harmful molecular mechanisms in sepsis. Nat Rev Immunol. 8:776-787.
79. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140.
80. Robinson MD, Oshlack A. 2010. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11:R25.
81. Rose E, Small CM, Saucedo HA, Harper C, Jones AG. 2014. Genetic evidence for monogamy in the dwarf seahorse, Hippocampus zosterae. J Hered. 105:828-833.
82. Saxena M, Yeretssian G. 2014. NOD-like receptors: master regulators of inflammation and cancer. Front Immunol. 5:327.
83. Schneider M, et al. 2012. The innate immune sensor NLRC3 attenuates toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-kappaB. Nat Immunol. 13:823-831.
84. Semova I, et al. 2012. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microb. 12:277-288.
85. Smith CC, Snowberg LK, Gregory Caporaso J, Knight R, Bolnick DI. 2015. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. isme J. 9:2515-2526.
86. Sommer F, Nookaew I, Sommer N, Fogelstrand P, Backhed F. 2015. Site-specific programming of the host epithelial transcriptome by the gut microbiota. Genome Biol. 16:62.
87. Stutz WE, Schmerer M, Coates JL, Bolnick DI. 2015. Among-lake reciprocal transplants induce convergent expression of immune genes in threespine stickleback. Mol Ecol. 24:4629-4646.
88. Sullam KE, et al. 2015. Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies. ISME J. 9:1508-1522.
89. van Nas A, et al. 2010. Expression quantitative trait loci: replication, tissue- and sex-specificity in mice. Genetics 185:1059-1068.
90. Wlodarska M, et al. 2014. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 156:1045-1059.
91. Wu TD, Nacu S. 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26:873-881.