title: Molecular signatures of nicotinoid-pathogen synergy in the termite gut.
abstract: Previous studies in lower termites revealed unexpected synergies between nicotinoid insecticides and fungal entomopathogens. The present study investigated molecular mechanisms of nicotinoid-pathogen synergy in the lower termite Reticulitermes flavipes, using the nicotinoid, imidacloprid, in combination with fungal and bacterial entomopathogens. Particular focus was placed on metatranscriptome composition and microbial dynamics in the symbiont-rich termite gut, which houses diverse mixes of protists and bacteria. cDNA microarrays containing a mix of host and protist symbiont oligonucleotides were used to simultaneously assess termite and protist gene expression. Five treatments were compared that included single challenges with sublethal doses of fungi (Metharizium anisopliae), bacteria (Serratia marcescens) or imidacloprid, and dual challenges with fungi + imidacloprid or bacteria + imidacloprid. Our findings point towards protist dysbiosis and compromised social behavior, rather than suppression of stereotypical immune defense mechanisms, as the dominant factors underlying nicotinoid-pathogen synergy in termites. Also, greater impacts observed for the fungal pathogen than for the bacterial pathogen suggest that the rich bacterial symbiont community in the R. flavipes gut (>5000 species-level phylotypes) exists in an ecological balance that effectively excludes exogenous bacterial pathogens. These findings significantly advance our understanding of antimicrobial defenses in this important eusocial insect group, as well as provide novel insights into how nicotinoids can exert deleterious effects on social insect colonies.
authors.affiliation: Dept. of Entomology, Purdue University, West Lafayette, IN, United States of America.
authors.forename: Ruchira
authors.initials: R
authors.lastname: Sen
authors.affiliation: Dept. of Entomology, Purdue University, West Lafayette, IN, United States of America.
authors.forename: Rhitoban
authors.initials: R
authors.lastname: Raychoudhury
authors.affiliation: Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, United States of America.
authors.forename: Yunpeng
authors.initials: Y
authors.lastname: Cai
authors.affiliation: Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, United States of America.
authors.forename: Yijun
authors.initials: Y
authors.lastname: Sun
authors.affiliation: Entomology and Nematology Department, University of Florida, Gainesville, FL, United States of America.
authors.forename: Verena-Ulrike
authors.initials: VU
authors.lastname: Lietze
authors.affiliation: Dept. of Entomology, Purdue University, West Lafayette, IN, United States of America.
authors.forename: Brittany F
authors.initials: BF
authors.lastname: Peterson
authors.affiliation: Dept. of Entomology, Purdue University, West Lafayette, IN, United States of America.
authors.forename: Michael E
authors.initials: ME
authors.lastname: Scharf
authors.affiliation: Entomology and Nematology Department, University of Florida, Gainesville, FL, United States of America.
authors.forename: Drion G
authors.initials: DG
authors.lastname: Boucias
mesh_terms: D000818:Animals; D004269:DNA, Bacterial / Q000235:genetics; D004271:DNA, Fungal / Q000235:genetics; D064806:Dysbiosis / Q000276:immunology / Q000382:microbiology; D005658:Fungi / Q000235:genetics*; D000069196:Gastrointestinal Microbiome / Q000187:drug effects; D041981:Gastrointestinal Tract / Q000382:microbiology; D007093:Imidazoles / Q000494:pharmacology*; D007306:Insecticides / Q000494:pharmacology*; D020049:Isoptera / Q000276:immunology / Q000382:microbiology*; D000073943:Neonicotinoids; D009574:Nitro Compounds / Q000494:pharmacology*; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017422:Sequence Analysis, DNA; D012706:Serratia marcescens / Q000235:genetics*; D013559:Symbiosis; D059467:Transcriptome / Q000235:genetics
chemical_list: D004269:DNA, Bacterial; D004271:DNA, Fungal; D007093:Imidazoles; D007306:Insecticides; D000073943:Neonicotinoids; D009574:Nitro Compounds; D012336:RNA, Ribosomal, 16S; C082359:imidacloprid
references.citation: Nat Rev Microbiol. 2014 Mar;12(3):168-80
references.pmid: 24487819
references.citation: Mol Ecol. 2013 Apr;22(7):1836-53
references.pmid: 23379767
references.citation: Biotechnol Biofuels. 2009 Oct 15;2:25
references.pmid: 19832970
references.citation: Front Zool. 2014 Mar 07;11(1):23
references.pmid: 24602309
references.citation: Nucleic Acids Res. 2008 Jun;36(10):3420-35
references.pmid: 18445632
references.citation: Mol Biol Evol. 2006 Feb;23(2):317-26
references.pmid: 16221893
references.citation: Insect Mol Biol. 2013 Apr;22(2):155-71
references.pmid: 23294456
references.citation: Naturwissenschaften. 1999 Nov;86(11):544-8
references.pmid: 10551951
references.citation: Peptides. 2009 May;30(5):855-60
references.pmid: 19428761
references.citation: J Biol Chem. 2001 Feb 9;276(6):4085-92
references.pmid: 11053427
references.citation: Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18466-71
references.pmid: 24145453
references.citation: BMC Mol Biol. 2010 Apr 23;11:28
references.pmid: 20416061
references.citation: Nucleic Acids Res. 2004 Jan 1;32(Database issue):D277-80
references.pmid: 14681412
references.citation: Front Microbiol. 2014 Nov 21;5:607
references.pmid: 25484878
references.citation: Microbiologyopen. 2014 Dec;3(6):910-21
references.pmid: 25257543
references.citation: Nat Genet. 2000 May;25(1):25-9
references.pmid: 10802651
references.citation: Arch Insect Biochem Physiol. 2013 Dec;84(4):175-93
references.pmid: 24186432
references.citation: Proc Natl Acad Sci U S A. 2002 May 14;99(10):6838-42
references.pmid: 12011442
references.citation: Insect Biochem Mol Biol. 2013 Jan;43(1):91-101
references.pmid: 23108206
references.citation: BMC Biol. 2007 Dec 21;5:56
references.pmid: 18154650
references.citation: Proc Biol Sci. 2013 Sep 18;280(1770):20131885
references.pmid: 24048157
references.citation: Science. 2013 May 10;340(6133):674-6
references.pmid: 23661734
references.citation: J Econ Entomol. 2003 Oct;96(5):1514-9
references.pmid: 14650526
references.citation: Naturwissenschaften. 2007 Jan;94(1):25-33
references.pmid: 16953417
references.citation: Appl Environ Microbiol. 2015 Feb;81(3):1059-70
references.pmid: 25452280
references.citation: Curr Biol. 2009 Jan 13;19(1):30-6
references.pmid: 19110429
references.citation: Mol Biol Evol. 2004 Dec;21(12):2256-64
references.pmid: 15317879
references.citation: PLoS One. 2014 Aug 20;9(8):e105582
references.pmid: 25141339
references.citation: J Med Microbiol. 2000 Jul;49(7):675-6
references.pmid: 10882095
references.citation: Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):12652-7
references.pmid: 19506247
references.citation: Annu Rev Pharmacol Toxicol. 2005;45:247-68
references.pmid: 15822177
references.citation: J Invertebr Pathol. 2008 Feb;97(2):165-70
references.pmid: 17949740
references.citation: PLoS One. 2012;7(1):e29268
references.pmid: 22235278
references.citation: Dev Comp Immunol. 2010 Apr;34(4):369-76
references.pmid: 19958789
references.citation: Peptides. 2010 Mar;31(3):419-28
references.pmid: 19747517
references.citation: PLoS Pathog. 2014 Mar 06;10(3):e1003897
references.pmid: 24603764
references.citation: J Econ Entomol. 2010 Jun;103(3):791-8
references.pmid: 20568625
references.citation: BMC Genomics. 2013 Jul 19;14:491
references.pmid: 23870282
references.citation: Methods Enzymol. 1999;303:179-205
references.pmid: 10349646
references.citation: Insect Biochem Mol Biol. 2007 Dec;37(12):1366-74
references.pmid: 17967355
references.citation: Nat Genet. 2002 Dec;32 Suppl:496-501
references.pmid: 12454644
references.citation: Gene. 2011 Mar 15;474(1-2):12-21
references.pmid: 21134424
references.citation: Dev Comp Immunol. 2002 Jul;26(6):495-503
references.pmid: 12031410
references.citation: PLoS One. 2013 Jul 16;8(7):e69543
references.pmid: 23874972