Composition, taxonomy and functional diversity of the oropharynx microbiome in individuals with schizophrenia and controls

PeerJ

Volumn 2015, Issue 8, 2015, Pages

  Castro Nallar, Eduardo ^a,f   Bendall, Matthew L ^a   Pérez Losada, Marcos ^a,e,g   Sabuncyan, Sarven ^b   Severance, Emily G ^b   Dickerson, Faith B ^c   Schroeder, Jennifer R ^d   Yolken, Robert H ^b   Crandall, Keith A ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHEPPARD PRATT HEALTH SYSTEM   (United States)

^d Schroeder Statistical Consulting   (United States)

^e UNIVERSITY OF PORTO   (Portugal)

^f UNIVERSIDAD ANDRÉS BELLO   (Chile)

^g CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Biomarkers; Functional diversity; Lactic acid bacteria; Metagenomics; Microbial abundance; Microbial diversity; Microbiome; PathoScope; Schizophrenia; Shotgun sequencing

Indexed keywords

CARBOHYDRATE; CYANOCOBALAMIN; GLUTAMIC ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SIDEROPHORE;

ACTINOBACTERIA; ACTINOMYCES; ADULT; ARTICLE; ASCOMYCETES; BACTEROIDETES; BIFIDOBACTERIUM; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM PSEUDOCATENULATUM; CANDIDA DUBLINIENSIS; CAPILLARY ELECTROPHORESIS; CATENIBACTERIUM MITSUOKAI; CHROMATOGRAPHY; CLINICAL ARTICLE; CONTROLLED STUDY; DNA EXTRACTION; ENERGY METABOLISM; ESCHERICHIA FERGUSONII; EUBACTERIUM HALII; FEMALE; FIRMICUTES; GENE SEQUENCE; HUMAN; INFLAMMATION; KLEBSIELLA VARIICOLA; LACTIC ACID BACTERIUM; LACTOBACILLI; LACTOBACILLUS GASSERI; LACTOBACILLUS SALIVARIUS; MALE; METABOLITE; MICROBIOME; NEISSERIA FLAVESCENS; NEISSERIA POLYSACCHAREA; NEISSERIA SUBFLAVA; NONHUMAN; OROPHARYNX; POLYMERASE CHAIN REACTION; PROTEOBACTERIA; PSEUDOMONAS PROTEGENS; SCHIZOPHRENIA; STREPTOCOCCUS; STREPTOCOCCUS GORDONII; STREPTOCOCCUS MITIS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS THERMOPHILUS; TAXONOMIC RANK; THROAT CULTURE;

ACTINOBACTERIA; ANIMALIA; ASCOMYCOTA; BACTEROIDETES; BIFIDOBACTERIUM; EUBACTERIUM HALLII; FIRMICUTES; PROTEOBACTERIA;

EID: 84940374210     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.1140     Document Type: Article

References (105)

1. Aagaard K, Riehle K, Ma J, Segata N, Mistretta T-A, Coarfa C, Raza S, Rosenbaum S, Van den Veyver I, Milosavljevic A. 2012. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS ONE 7:e36466 DOI 10.1371/journal.pone.0036466.
2. Achim AM, Ouellet R, Lavoie M-A, Vallières C, Jackson PL, Roy M-A. 2013. Impact of social anxiety on social cognition and functioning in patients with recent-onset schizophrenia spectrum disorders. Schizophrenia Research 145:75-81 DOI 10.1016/j.schres.2013.01.012.
3. American Psychiatric Association. 2000. Diagnostic and statistical manual of mental disorders, text revision (DSM-IV-TR). Washington, D.C.: American Psychiatric Association.
4. Andreassen O, Harbo H, Wang Y, Thompson W, Schork A, Mattingsdal M, Zuber V, Bettella F, Ripke S, Kelsoe J. 2014. Genetic pleiotropy between multiple sclerosis and schizophrenia but not bipolar disorder: differential involvement of immune-related gene loci. Molecular Psychiatry 10:207-214 DOI 10.1038/mp.2013.195.
5. Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R, Romero H, Simón-Soro A, Pignatelli M, Mira A. 2011. The oral metagenome in health and disease. The ISME Journal 6:46-56 DOI 10.1038/ismej.2011.85.
6. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57:289-300.
7. Benros ME, Nielsen PR, Nordentoft M, Eaton WW, Dalton SO, Mortensen PB. 2014. Autoimmune diseases and severe infections as risk factors for schizophrenia: a 30-year population-based register study. American Journal of Psychiatry 168:1303-1310 DOI 10.1176/appi.ajp.2011.11030516.
8. Bercik P, Verdu EF, Foster JA, Macri J, Potter M, Huang X, Malinowski P, Jackson W, Blennerhassett P, Neufeld KA. 2010. Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology 139:2102-2112 DOI 10.1053/j.gastro.2010.06.063.
9. Bisgaard H, Hermansen MN, Buchvald F, Loland L, Halkjaer LB, Bønnelykke K, Brasholt M, Heltberg A, Vissing NH, Thorsen SV. 2007. Childhood asthma after bacterialcolonization of the airway in neonates. New England Journal of Medicine 357:1487-1495 DOI 10.1056/NEJMoa052632.
10. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences of the United States of America 108:16050-16055 DOI 10.1073/pnas.1102999108.
11. Brook I, Gober AE. 2005. Recovery of potential pathogens and interfering bacteria in the nasopharynx of smokers and nonsmokers. CHEST Journal 127:2072-2075 DOI 10.1378/chest.127.6.2072.
12. Castro-Nallar E, Shen Y, Freishtat RJ, Perez-Losada M, Manimaran S, Liu G, Johnson WE, Crandall KA. 2015. Integrating microbial and host transcriptomics to characterize asthma-associated microbial communities. BMC Medical Genomics In Press.
13. Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11:265-270.
14. Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, Hwang J, Bushman FD, Collman RG. 2010. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS ONE 5:e15216 DOI 10.1371/journal.pone.0015216.
15. Cho I, Blaser MJ. 2012. The human microbiome: at the interface of health and disease. Nature Reviews Genetics 13:260-270 DOI 10.1038/nrg3182.
16. Clark RB, Cervantes JL, Maciejewski MW, Farrokhi V, Nemati R, Yao X, Anstadt E, Fujiwara M, Wright KT, Riddle C. 2013. Serine lipids of Porphyromonas gingivalis are human and mouse Toll-like receptor 2 ligands. Infection and Immunity 81:3479-3489 DOI 10.1128/IAI.00803-13.
17. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney R, Shanahan F, Dinan T, Cryan J. 2012. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Molecular Psychiatry 18:666-673 DOI 10.1038/mp.2012.77.
18. Colwell RK, Coddington JA. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 345:101-118 DOI 10.1098/rstb.1994.0091.
19. Cook RD. 1977. Detection of influential observation in linear regression. Technometrics 19:15-18 DOI 10.2307/1268249.
20. Dal Bello F, Hertel C. 2006. Oral cavity as natural reservoir for intestinal Lactobacilli. Systematic and applied microbiology 29:69-76 DOI 10.1016/j.syapm.2005.07.002.
21. Davari S, Talaei S, Alaei H. 2013. Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome-gut-brain axis. Neuroscience 240:287-296 DOI 10.1016/j.neuroscience.2013.02.055.
22. De Vos WM, De Vos EA. 2012. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutrition Reviews 70:S45-S56 DOI 10.1111/j.1753-4887.2012.00505.x.
23. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, YuW-H, Lakshmanan A, WadeWG. 2010. The human oral microbiome. Journal of Bacteriology 192:5002-5017 DOI 10.1128/JB.00542-10.
24. Dickerson F, Stallings C, Origoni A, Vaughan C, Khushalani S, Yang S, Yolken R. 2013. C-reactive protein is elevated in schizophrenia. Schizophrenia Research 143:198-202 DOI 10.1016/j.schres.2012.10.041.
25. Dillon VM. 1998. Lactic acid bacteria: microbiology and functional aspects. International Journal of Food Science & Technology 33:195-196 DOI 10.1046/j.1365-2621.1998.33201914.x.
26. Dinan T, Borre Y, Cryan J. 2014. Genomics of schizophrenia: time to consider the gut microbiome? Molecular Psychiatry 19:1252-1257 DOI 10.1038/mp.2014.93.
27. Ding T, Schloss PD. 2014. Dynamics and associations of microbial community types across the human body. Nature 509:357-360 DOI 10.1038/nature13178.
28. Docktor MJ, Paster BJ, Abramowicz S, Ingram J, Wang YE, Correll M, Jiang H, Cotton SL, Kokaras AS, Bousvaros A. 2012. Alterations in diversity of the oral microbiome in pediatric inflammatory bowel disease. Inflammatory Bowel Diseases 18:935-942 DOI 10.1002/ibd.21874.
29. Duncan SH, Louis P, Flint HJ. 2004. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Applied and Environmental Microbiology 70:5810-5817 DOI 10.1128/AEM.70.10.5810-5817.2004.
30. Eaton WW, Pedersen MG, Nielsen PR, Mortensen PB. 2010. Autoimmune diseases, bipolar disorder, and non-affective psychosis. Bipolar Disorders 12:638-646 DOI 10.1111/j.1399-5618.2010.00853.x.
31. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461 DOI 10.1093/bioinformatics/btq461.
32. Eggimann P, Pittet D. 2014. Candida colonization index and subsequent infection in critically ill surgical patients: 20 years later. Intensive Care Medicine 40:1429-1448 DOI 10.1007/s00134-014-3355-z.
33. Falkai P, Schmitt A, Cannon TD. 2011. Pathophysiology of schizophrenia. Chichester: John Wiley & Sons, Ltd.
34. Farrokhi V, Nemati R, Nichols FC, Yao X, Anstadt E, Fujiwara M, Grady J, Wakefield D, Castro W, Donaldson J. 2013. Bacterial lipodipeptide, Lipid 654, is a microbiome-associated biomarker for multiple sclerosis. Clinical & Translational Immunology 2:e8 DOI 10.1038/cti.2013.11.
35. First MB, Spitzer RL, Gibbon M, Williams JB. 2012. Structured clinical interview for DSM-IV® Axis I disorders (SCID-I), clinician version, administration booklet. Washington, D.C.: American Psychiatric Association.
36. Foster JA, McVey Neufeld K-A. 2013. Gut-brain axis: how the microbiome influences anxiety and depression. Trends in Neurosciences 36:305-312 DOI 10.1016/j.tins.2013.01.005.
37. Fowler T, Zammit S, Owen MJ, Rasmussen F. 2012. A population-based study of shared genetic variation between premorbid IQ and psychosis among male twin pairs and sibling pairs from Sweden. Archives of General Psychiatry 69:460-466 DOI 10.1001/archgenpsychiatry.2011.1370.
38. Francis OE, Bendall M, Manimaran S, Hong C, Clement NL, Castro-Nallar E, Snell Q, Schaalje GB, Clement MJ, Crandall KA. 2013. Pathoscope: species identification and strain attribution with unassembled sequencing data. Genome Research 23:1721-1729 DOI 10.1101/gr.150151.112.
39. Franzosa EA, Morgan XC, Segata N, Waldron L, Reyes J, Earl AM, Giannoukos G, Boylan MR, Ciulla D, Gevers D. 2014. Relating the metatranscriptome and metagenome of the human gut. Proceedings of the National Academy of Sciences of the United States of America 111:E2329-E2338 DOI 10.1073/pnas.1319284111.
40. Gao Z, Kang Y, Yu J, Ren L. 2014. Human pharyngeal microbiome may play a protective role in respiratory tract infections. Genomics, Proteomics & Bioinformatics 12:144-150 DOI 10.1016/j.gpb.2014.06.001.
41. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5:R80 DOI 10.1186/gb-2004-5-10-r80.
42. Gevers D, Kugathasan S, Denson LA, Vázquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M. 2014. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host & Microbe 15:382-392 DOI 10.1016/j.chom.2014.02.005.
43. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, Gillevet PM. 2010. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathogens 6:e1000713 DOI 10.1371/journal.ppat.1000713.
44. Haberman Y, Tickle TL, Dexheimer PJ, Kim M-O, Tang D, Karns R, Baldassano RN, Noe JD, Rosh J, Markowitz J. 2014. Pediatric Crohn disease patients exhibit specific ileal transcriptome and microbiome signature. The Journal of Clinical Investigation 124(8):3617-3633 DOI 10.1172/JCI75436.
45. Hong P-Y, Lee BW, Aw M, Shek LPC, Yap GC, Chua KY, LiuW-T. 2010. Comparative analysis of fecal microbiota in infants with and without eczema. PLoS ONE 5:e9964 DOI 10.1371/journal.pone.0009964.
46. Hong C, Manimaran S, Shen Y, Perez-Rogers JF, Byrd AL, Castro-Nallar E, Crandall KA, Johnson WE. 2014. PathoScope 2.0: a complete computational framework for strain identification in environmental or clinical sequencing samples. Microbiome 2:1-15 DOI 10.1186/2049-2618-2-33.
47. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF. 2013. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:1451-1463 DOI 10.1016/j.cell.2013.11.024.
48. Huang YJ. 2013. Asthma microbiome studies and the potential for new therapeutic strategies. Current Allergy and Asthma Reports 13:453-461 DOI 10.1007/s11882-013-0355-y.
49. Jakobsson HE, Jernberg C, Andersson AF, Sjölund-Karlsson M, Jansson JK, Engstrand L. 2010. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS ONE 5:e9836 DOI 10.1371/journal.pone.0009836.
50. Jost L. 2007. Partitioning diversity into independent alpha and beta components. Ecology 88:2427-2439 DOI 10.1890/06-1736.1.
51. Kageyama A, Benno Y. 2000. Catenibacterium mitsuokai gen. nov., sp. nov., a gram-positive anaerobic bacterium isolated from human faeces. International Journal of Systematic and Evolutionary Microbiology 50:1595-1599 DOI 10.1099/00207713-50-4-1595.
52. Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28:27-30 DOI 10.1093/nar/28.1.27.
53. Kang D-W, Park JG, Ilhan ZE, WallstromG, LaBaer J, Adams JB, Krajmalnik-Brown R. 2013. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS ONE 8:e68322 DOI 10.1371/journal.pone.0068322.
54. Kennedy JL, Altar CA, Taylor DL, Degtiar I, Hornberger JC. 2014. The social and economic burden of treatment-resistant schizophrenia: a systematic literature review. International Clinical Psychopharmacology 29:63-76 DOI 10.1097/YIC.0b013e32836508e6.
55. Kim J, Sudbery P. 2011. Candida albicans, a major human fungal pathogen. The Journal of Microbiology 49:171-177 DOI 10.1007/s12275-011-1064-7.
56. Knapp M, Mangalore R, Simon J. 2004. The global costs of schizophrenia. Schizophrenia Bulletin 30(2):279-293 DOI 10.1093/oxfordjournals.schbul.a007078.
57. Kriegel MA, Sefik E, Hill JA, Wu H-J, Benoist C, Mathis D. 2011. Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proceedings of the National Academy of Sciences of the United States of America 108:11548-11553 DOI 10.1073/pnas.1108924108.
58. Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK. 2005. Lactobacillus sepsis associated with probiotic therapy. Pediatrics 115:178-181.
59. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9:357-359 DOI 10.1038/nmeth.1923.
60. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biology 15(2):550 DOI 10.1186/s13059-014-0550-8.
61. Lukens JR, Gurung P, Vogel P, Johnson GR, Carter RA, McGoldrick DJ, Bandi SR, Calabrese CR, Walle LV, Lamkanfi M. 2014. Dietary modulation of the microbiome affects autoinflammatory disease. Nature 516:246-249 DOI 10.1038/nature13788.
62. Luongo D, Miyamoto J, Bergamo P, Nazzaro F, Baruzzi F, Sashihara T, Tanabe S, Rossi M. 2013. Differential modulation of innate immunity in vitro by probiotic strains of Lactobacillus gasseri. BMC Microbiology 13:298 DOI 10.1186/1471-2180-13-298.
63. Lusk RW. 2014. Diverse and widespread contamination evident in the unmapped depths of high throughput sequencing data. PLoS ONE 9:e110808 DOI 10.1371/journal.pone.0110808.
64. Martin FPJ, Wang Y, Sprenger N, Yap IK, Lundstedt T, Lek P, Rezzi S, Ramadan Z, Van Bladeren P, Fay LB. 2008. Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Molecular Systems Biology 4:157 DOI 10.1038/msb4100190.
65. McMurdie PJ, Holmes S. 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217 DOI 10.1371/journal.pone.0061217.
66. Meehan CJ, Beiko RG. 2012. Lateral gene transfer of an ABC transporter complex between major constituents of the human gut microbiome. BMC Microbiology 12:248 DOI 10.1186/1471-2180-12-248.
67. Merchant S, Wood DE, Salzberg SL. 2014. Unexpected cross-species contamination in genome sequencing projects. PeerJ 2:e675 DOI 10.7717/peerj.675.
68. Molyneaux PL, Mallia P, Cox MJ, Footitt J, Willis-Owen SA, Homola D, Trujillo-Torralbo M-B, Elkin S, Kon OM, CooksonWO. 2013. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine 188:1224-1231 DOI 10.1164/rccm.201302-0341OC.
69. Morgan XC, Kabakchiev B, Waldron L, Tyler AD, Tickle TL, MilgromR, Stempak JM, Gevers D, Xavier RJ, Silverberg MS. 2015. Associations between host gene expression, the mucosal microbiome, and clinical outcome in the pelvic pouch of patients with inflammatory bowel disease. Genome Biology 16:67 DOI 10.1186/s13059-015-0637-x.
70. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB. 2012. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biology 13:R79 DOI 10.1186/gb-2012-13-9-r79.
71. Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, Flores SC, Fontenot AP, Ghedin E, Huang L. 2013. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. American Journal of Respiratory and Critical Care Medicine 187:1067-1075 DOI 10.1164/rccm.201210-1913OC.
72. Nakayama J, Kobayashi T, Tanaka S, Korenori Y, Tateyama A, Sakamoto N, Kiyohara C, Shirakawa T, Sonomoto K. 2011. Aberrant structures of fecal bacterial community in allergic infants profiled by 16S rRNA gene pyrosequencing. FEMS Immunology & Medical Microbiology 63:397-406 DOI 10.1111/j.1574-695X.2011.00872.x.
73. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. 2014. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123-3124 DOI 10.1093/bioinformatics/btu494.
74. Pérez-Losada M, Castro-Nallar E, Bendall M, Freishtat RJ, Crandall KA. 2015. Dual transcriptomic profiling of host and microbiota during health and disease in pediatric asthma. PLoS ONE 10(6):e0131819 DOI 10.1371/journal.pone.0131819.
75. Pflughoeft KJ, Versalovic J. 2012. Human microbiome in health and disease. Annual Review of Pathology: Mechanisms of Disease 7:99-122 DOI 10.1146/annurev-pathol-011811-132421.
76. Reuter G. 2001. The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Current Issues in Intestinal Microbiology 2:43-53.
77. Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nature Reviews Immunology 9:313-323 DOI 10.1038/nri2515.
78. Salter SJ, Cox MJ, Turek EM, Calus ST, CooksonWO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW. 2014. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biology 12:87 DOI 10.1186/s12915-014-0087-z.
79. Scher JU, Abramson SB. 2011. The microbiome and rheumatoid arthritis. Nature Reviews Rheumatology 7:569-578 DOI 10.1038/nrrheum.2011.121.
80. SchizophreniaWorking Group of the Psychiatric Genomics Consortium. 2014. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511:421-427 DOI 10.1038/nature13595.
81. Sczesnak A, Segata N, Qin X, Gevers D, Petrosino JF, Huttenhower C, Littman DR, Ivanov II. 2011. The genome of th17 cell-inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment. Cell Host & Microbe 10:260-272 DOI 10.1016/j.chom.2011.08.005.
82. Sebti A, Kiehn TE, Perlin D, Chaturvedi V, Wong M, Doney A, Park S, Sepkowitz KA. 2001. Candida dubliniensis at a cancer center. Clinical Infectious Diseases 32:1034-1038 DOI 10.1086/319599.
83. Seekatz AM, Aas J, Gessert CE, Rubin TA, Saman DM, Bakken JS, Young VB. 2014. Recovery of the gut microbiome following fecal microbiota transplantation. mBio 5:e00893-14 DOI 10.1128/mBio.00893-14.
84. Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, Huttenhower C, Izard J. 2012. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biology 13:R42 DOI 10.1186/gb-2012-13-6-r42.
85. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, GarrettWS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology 12:R60 DOI 10.1186/gb-2011-12-6-r60.
86. Selle K, Klaenhammer TR. 2013. Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiology Reviews 37:915-935 DOI 10.1111/1574-6976.12021.
87. Severance EG, Gressitt KL, Stallings CR, Origoni AE, Khushalani S, Leweke FM, Dickerson FB, Yolken RH. 2013. Discordant patterns of bacterial translocation markers and implications for innate immune imbalances in schizophrenia. Schizophrenia Research 148:130-137 DOI 10.1016/j.schres.2013.05.018.
88. Severance EG, Yolken RH, Eaton WW. 2014. Autoimmune diseases, gastrointestinal disorders and the microbiome in schizophrenia: more than a gut feeling. Schizophrenia Research 14:319-313 DOI 10.1016/j.schres.2014.06.027.
89. Shoemark DK, Allen SJ. 2014. The microbiome and disease: reviewing the links between the oral microbiome, aging, and Alzheimer's disease. Journal of Alzheimer's Disease 43:725-738 DOI 10.3233/JAD-141170.
90. Storey JD, Taylor JE, Siegmund D. 2004. Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 66:187-205 DOI 10.1111/j.1467-9868.2004.00439.x.
91. Strong MJ, Xu G, Morici L, Bon-Durant SS, Baddoo M, Lin Z, Fewell C, Taylor CM, Flemington EK. 2014. Microbial contamination in next generation sequencing: implications for sequence-based analysis of clinical samples. PLoS Pathogens 10:e1004437 DOI 10.1371/journal.ppat.1004437.
92. Suez J, KoremT, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, Israeli D, Zmora N, Gilad S, Weinberger A. 2014. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514:181-186 DOI 10.1038/nature13793.
93. Tienari P, Sorri A, Lahti I, Naarala M, Wahlberg K, Rönkkö T, Pohjola J, Moring J. 1985. The Finnish adoptive family study of schizophrenia. The Yale Journal of Biology and Medicine 58:227-237.
94. 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 444:1027-1131 DOI 10.1038/nature05414.
95. Van Os J, Kenis G, Rutten BP. 2010. The environment and schizophrenia. Nature 468:203-212 DOI 10.1038/nature09563.
96. Voss M, Wonnenberg B, Honecker A, Kamyschnikow A, Herr C, Bischoff M, Tschernig T, Bals R, Beisswenger C. 2015. Cigarette smoke-promoted acquisition of bacterial pathogens in the upper respiratory tract leads to enhanced inflammation in mice. Respiratory Research 16:41 DOI 10.1186/s12931-015-0204-8.
97. Weinstock GM. 2012. Genomic approaches to studying the human microbiota. Nature 489:250-256 DOI 10.1038/nature11553.
98. Weiss S, Amir A, Hyde ER, Metcalf JL, Song SJ, Knight R. 2014. Tracking down the sources of experimental contamination in microbiome studies. Genome Biology 15:564 DOI 10.1186/s13059-014-0564-2.
99. White JR, Nagarajan N, Pop M. 2009. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Computational Biology 5:e1000352 DOI 10.1371/journal.pcbi.1000352.
100. Wickham H. 2009. ggplot2: elegant graphics for data analysis. New York: Springer.
101. Wu H-J, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, Littman DR, Benoist C, Mathis D. 2010. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32:815-827 DOI 10.1016/j.immuni.2010.06.001.
102. Ye Y, Doak TG. 2009. A parsimony approach to biological pathway reconstruction/inference for genomes and metagenomes. PLoS Computational Biology 5:e1000465 DOI 10.1371/journal.pcbi.1000465.
103. Yokote H, Miyake S, Croxford JL, Oki S, Mizusawa H, Yamamura T. 2008. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. The American Journal of Pathology 173:1714-1723 DOI 10.2353/ajpath.2008.080622.
104. Yolken R, Dickerson F. 2014. The microbiome: the missing link in the pathogenesis of schizophrenia. Neurology, Psychiatry and Brain Research 20:26-27 DOI 10.1016/j.npbr.2014.01.177.
105. Yolken RH, Severance EG, Sabunciyan S, Gressitt KL, Chen O, Stallings C, Origoni A, Katsafanas E, Schweinfurth LA, Savage CL. 2015. Metagenomic sequencing indicates that the oropharyngeal phageome of individuals with schizophrenia differs from that of controls. Schizophrenia Bulletin 41(5):1153-1161 DOI 10.1093/schbul/sbu197.