The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila.
Insulin/IGF-like signalling (IIS) is an evolutionarily conserved pathway that has diverse functions in multi-cellular organisms. Mutations that reduce IIS can have pleiotropic effects on growth, development, metabolic homeostasis, fecundity, stress resistance and lifespan. IIS is also modified by extrinsic factors. For instance, in the fruitfly Drosophila melanogaster, both nutrition and stress can alter the activity of the pathway. Here, we test experimentally the hypothesis that a widespread endosymbiont of arthropods, Wolbachia pipientis, can alter the degree to which mutations in genes encoding IIS components affect IIS and its resultant phenotypes. Wolbachia infection, which is widespread in D. melanogaster in nature and has been estimated to infect 30 per cent of strains in the Bloomington stock centre, can affect broad aspects of insect physiology, particularly traits associated with reproduction. We measured a range of IIS-related phenotypes in flies ubiquitously mutant for IIS in the presence and absence of Wolbachia. We show that removal of Wolbachia further reduces IIS and hence enhances the mutant phenotypes, suggesting that Wolbachia normally acts to increase insulin signalling. This effect of Wolbachia infection on IIS could have an evolutionary explanation, and has some implications for studies of IIS in Drosophila and other organisms that harbour endosymbionts.
Ikeya
Tomoatsu
T
UCL Institute of Healthy Ageing and GEE, University College London, Darwin Building, Gower Street, London, UK.
Broughton
Susan
S
Alic
Nazif
N
Grandison
Richard
R
Partridge
Linda
L
D000818:Animals; D004331:Drosophila melanogaster / Q000378:metabolism* / Q000382:microbiology*; D005216:Fat Body / Q000378:metabolism; D005786:Gene Expression Regulation; D007328:Insulin / Q000378:metabolism*; D009154:Mutation; D015398:Signal Transduction; D013002:Somatomedins / Q000378:metabolism*; D020577:Wolbachia / Q000502:physiology*
D007328:Insulin; D013002:Somatomedins
Curr Biol. 2004 May 25;14(10):885-90
15186745
Heredity (Edinb). 2001 Jun;86(Pt 6):731-7
11595053
Curr Opin Microbiol. 2004 Feb;7(1):67-70
15036143
Genes Dev. 2003 Aug 15;17(16):2006-20
12893776
Genetics. 1996 Nov;144(3):1063-73
8913750
Exp Gerontol. 2003 Nov-Dec;38(11-12):1353-64
14698816
Science. 2001 Apr 6;292(5514):104-6
11292874
Cell. 2005 Apr 8;121(1):115-25
15820683
Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3105-10
15708981
Nature. 2001 Dec 13;414(6865):799-806
11742412
Heredity (Edinb). 2004 Oct;93(4):379-89
15305172
PLoS Biol. 2007 May;5(5):e114
17439303
J Intern Med. 2008 Feb;263(2):179-91
18226095
Genetics. 2000 Oct;156(2):699-709
11014817
Annu Rev Microbiol. 1999;53:71-102
10547686
Genetics. 2003 Jun;164(2):545-52
12807775
FASEB J. 2008 Mar;22(3):807-18
17928362
Development. 2004 Aug;131(16):3897-906
15253933
Science. 2007 Jul 20;317(5836):369-72
17641201
Curr Biol. 2006 Oct 24;16(20):1977-85
17055976
N Engl J Med. 2001 Nov 8;345(19):1359-67
11794168
Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12602-7
11675496
Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4494-9
15767565
Nature. 2003 Jan 9;421(6919):182-7
12483226
Nature. 2007 Jan 18;445(7125):275-80
17136098
Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15911-5
17043223
Aging Cell. 2008 Oct;7(5):758-70
18691185
Nature. 2003 Dec 11;426(6967):620
14668850
Am J Physiol Endocrinol Metab. 2000 Jul;279(1):E206-12
10893341
Genetics. 1998 Jan;148(1):221-31
9475734
Science. 2001 Apr 6;292(5514):107-10
11292875
Aging Cell. 2007 Aug;6(4):429-38
17465980
Curr Biol. 2002 Aug 6;12(15):1293-300
12176357
Genes Dev. 2007 Mar 15;21(6):632-7
17369395
Genes Dev. 1999 Dec 15;13(24):3244-58
10617573
J Biol. 2003;2(3):20
12908874
Science. 2003 Feb 28;299(5611):1346-51
12610294
Annu Rev Physiol. 2001;63:141-64
11181952
Science. 2004 Jul 16;305(5682):361
15192154
Trends Endocrinol Metab. 2009 Apr;20(3):100-6
19251431
Cell. 1999 Jun 25;97(7):865-75
10399915
Insect Mol Biol. 2007 Dec;16(6):799-802
18093008
PLoS Genet. 2007 Jun;3(6):e95
17571923
Proc Biol Sci. 1998 Mar 22;265(1395):509-15
9569669
Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7540-4
7638227
Genet Res. 1993 Aug;62(1):23-9
7691685
PLoS Pathog. 2009 Apr;5(4):e1000368
19343208
Endocrinology. 2008 Jun;149(6):2714-23
18325986
Dev Cell. 2004 Aug;7(2):167-78
15296714
Proc Natl Acad Sci U S A. 2005 Sep 13;102(37):13289-94
16150727
Science. 2002 Mar 15;295(5562):2088-91
11872800
Science. 2002 May 10;296(5570):1118-20
12004130
Nature. 2002 Jul 4;418(6893):76-9
12097909
Nat Rev Genet. 2002 Mar;3(3):165-75
11972154
Sci Aging Knowledge Environ. 2002 May 22;2002(20):pe6
14602988
Science. 1997 Aug 15;277(5328):942-6
9252323
Science. 2003 Sep 19;301(5640):1731-3
14500985
J Gerontol A Biol Sci Med Sci. 2007 Oct;62(10):1071-81
17921418
Nature. 2004 Jun 3;429(6991):562-6
15175753
Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12596-601
11675495
Biol Bull. 1999 Oct;197(2):198-206
10573839
Genetics. 2005 Aug;170(4):1667-75
15937134
Curr Biol. 2003 Apr 1;13(7):603-6
12676093
J Am Diet Assoc. 2008 Apr;108(4 Suppl 1):S24-8
18358250
Genes Dev. 2003 Apr 1;17(7):813-8
12670864
Science. 2005 Feb 18;307(5712):1098-101
15718470
Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10792-6
9380712
J Biol Chem. 1997 Oct 3;272(40):25289-95
9312146
Curr Diabetes Rev. 2007 Aug;3(3):176-84
18220669
Cell. 2006 Feb 10;124(3):471-84
16469695
FEBS Lett. 2004 May 7;565(1-3):43-7
15135050
Curr Biol. 2001 Feb 20;11(4):213-21
11250149