Large-Scale Phylogenetic Analysis of Trypanosomatid Adenylate Cyclases Reveals Associations with Extracellular Lifestyle and Host-Pathogen Interplay.
Kinetoplastida
adenylate cyclase
oxygen
phylogenetics
receptor
trypanosomatid
Journal
Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707
Informations de publication
Date de publication:
06 12 2020
06 12 2020
Historique:
accepted:
21
10
2020
pubmed:
27
10
2020
medline:
6
10
2021
entrez:
26
10
2020
Statut:
ppublish
Résumé
Receptor adenylate cyclases (RACs) on the surface of trypanosomatids are important players in the host-parasite interface. They detect still unidentified environmental signals that affect the parasites' responses to host immune challenge, coordination of social motility, and regulation of cell division. A lesser known class of oxygen-sensing adenylate cyclases (OACs) related to RACs has been lost in trypanosomes and expanded mostly in Leishmania species and related insect-dwelling trypanosomatids. In this work, we have undertaken a large-scale phylogenetic analysis of both classes of adenylate cyclases (ACs) in trypanosomatids and the free-living Bodo saltans. We observe that the expanded RAC repertoire in trypanosomatids with a two-host life cycle is not only associated with an extracellular lifestyle within the vertebrate host, but also with a complex path through the insect vector involving several life cycle stages. In Trypanosoma brucei, RACs are split into two major clades, which significantly differ in their expression profiles in the mammalian host and the insect vector. RACs of the closely related Trypanosoma congolense are intermingled within these two clades, supporting early RAC diversification. Subspecies of T. brucei that have lost the capacity to infect insects exhibit high numbers of pseudogenized RACs, suggesting many of these proteins have become redundant upon the acquisition of a single-host life cycle. OACs appear to be an innovation occurring after the expansion of RACs in trypanosomatids. Endosymbiont-harboring trypanosomatids exhibit a diversification of OACs, whereas these proteins are pseudogenized in Leishmania subgenus Viannia. This analysis sheds light on how ACs have evolved to allow diverse trypanosomatids to occupy multifarious niches and assume various lifestyles.
Identifiants
pubmed: 33104188
pii: 5940001
doi: 10.1093/gbe/evaa226
pmc: PMC7719234
doi:
Substances chimiques
Adenylyl Cyclases
EC 4.6.1.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2403-2416Informations de copyright
© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
PLoS One. 2012;7(5):e36619
pubmed: 22574199
Mol Microbiol. 2012 Apr;84(2):225-42
pubmed: 22340731
Bioinformatics. 2001 Aug;17(8):754-5
pubmed: 11524383
Nat Commun. 2019 Feb 18;10(1):803
pubmed: 30778051
Lancet. 2017 Nov 25;390(10110):2397-2409
pubmed: 28673422
Eur J Biochem. 2001 Dec;268(23):6197-206
pubmed: 11733015
Cell Rep. 2016 Oct 11;17(3):660-670
pubmed: 27732844
Mol Cell Proteomics. 2015 Jul;14(7):1977-88
pubmed: 25963835
mBio. 2015 Apr 28;6(3):e01954-14
pubmed: 25922395
Curr Biol. 2016 Jan 25;26(2):161-172
pubmed: 26725202
J Infect Dis. 2012 Jul 15;206(2):229-37
pubmed: 22291195
Pathogens. 2018 Apr 25;7(2):
pubmed: 29693583
Nucleic Acids Res. 2006;34(14):4012-24
pubmed: 16914442
Pathogens. 2019 Nov 17;8(4):
pubmed: 31744234
F1000Res. 2017 May 16;6:
pubmed: 28620452
Biochim Biophys Acta. 2013 Jul;1834(7):1271-8
pubmed: 23535202
Folia Parasitol (Praha). 2017 Jul 10;64:
pubmed: 28783029
J Biol Chem. 2013 Sep 13;288(37):26914-25
pubmed: 23893410
PLoS Pathog. 2015 Jan 21;11(1):e1004484
pubmed: 25607944
Mol Biochem Parasitol. 2016 Mar-Apr;206(1-2):13-9
pubmed: 26975431
PLoS Negl Trop Dis. 2015 Jan 08;9(1):e3404
pubmed: 25568942
Open Biol. 2012 Feb;2(2):110037
pubmed: 22645659
PLoS One. 2015 Jun 18;10(6):e0130099
pubmed: 26086767
Protist. 2014 Sep;165(5):594-604
pubmed: 25113831
PLoS Genet. 2014 Feb 06;10(2):e1004007
pubmed: 24516393
Eukaryot Cell. 2014 Aug;13(8):1064-76
pubmed: 24879126
Proc Natl Acad Sci U S A. 2013 Oct 15;110(42):16790-5
pubmed: 24082109
Infect Immun. 2008 Oct;76(10):4757-63
pubmed: 18694966
mBio. 2016 Mar 15;7(2):e01985
pubmed: 26980834
Int J Parasitol. 2002 Aug;32(9):1071-84
pubmed: 12117490
Cell Host Microbe. 2016 Jun 8;19(6):837-48
pubmed: 27237364
J Biol Chem. 1995 Jul 21;270(29):17551-8
pubmed: 7615561
Antimicrob Agents Chemother. 2013 Oct;57(10):4882-93
pubmed: 23877697
Microbes Infect. 2010 Sep;12(10):716-26
pubmed: 20466066
Curr Biol. 2013 Sep 23;23(18):1787-93
pubmed: 24012313
Science. 2012 Jul 27;337(6093):463-6
pubmed: 22700656
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Trends Parasitol. 2018 Jun;34(6):466-480
pubmed: 29605546
Pathogens. 2020 Jul 15;9(7):
pubmed: 32679679
Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10140-4
pubmed: 8234267
Mol Cell Biol. 1992 Mar;12(3):1218-25
pubmed: 1545803
PLoS Negl Trop Dis. 2014 Sep 18;8(9):e3176
pubmed: 25233456
Biol Rev Camb Philos Soc. 2013 Aug;88(3):645-68
pubmed: 23356492
Nat Biotechnol. 2019 Apr;37(4):420-423
pubmed: 30778233
Mol Biochem Parasitol. 2017 Jan;211:67-70
pubmed: 27984073
Kinetoplastid Biol Dis. 2002 Jul 5;1(1):5
pubmed: 12234384
Nat Commun. 2019 Mar 29;10(1):1421
pubmed: 30926779
BMC Bioinformatics. 2008 Sep 23;9:392
pubmed: 18811934
Trends Parasitol. 2013 Jan;29(1):43-52
pubmed: 23246083
Sci Data. 2014 Aug 05;1:140024
pubmed: 25977781
Nucleic Acids Res. 2019 Jul 2;47(W1):W636-W641
pubmed: 30976793
Front Cell Infect Microbiol. 2016 Sep 28;6:115
pubmed: 27734008
Proc Natl Acad Sci U S A. 2012 Sep 4;109(36):14399-404
pubmed: 22908264
Adv Parasitol. 2017;98:283-309
pubmed: 28942771
Mol Biol Evol. 2016 Aug;33(8):2163-6
pubmed: 27189561
J Mol Biol. 2001 Jan 19;305(3):567-80
pubmed: 11152613
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
FASEB J. 2007 Mar;21(3):720-31
pubmed: 17167070
Mol Biochem Parasitol. 2014 Jul;195(2):115-22
pubmed: 24893339
J Eukaryot Microbiol. 2016 Sep;63(5):657-78
pubmed: 27009761
PLoS Negl Trop Dis. 2013;7(3):e2121
pubmed: 23556014
Physiol Rev. 2014 Jul;94(3):739-77
pubmed: 24987004
Cell. 2019 Jan 10;176(1-2):306-317.e16
pubmed: 30503212
Science. 2005 Jul 15;309(5733):404-9
pubmed: 16020724
Eukaryot Cell. 2015 Jan;14(1):104-12
pubmed: 25416239
Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):1999-2004
pubmed: 18245376
Trends Parasitol. 2015 Aug;31(8):373-9
pubmed: 26004537
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Exp Parasitol. 1995 Dec;81(4):618-20
pubmed: 8543006
Parasitology. 2019 Jan;146(1):1-27
pubmed: 29898792
Open Biol. 2015 Jan;5(1):140197
pubmed: 25567099
Nucleic Acids Res. 2014 Apr;42(6):3623-37
pubmed: 24442674
Mol Biol Evol. 2013 May;30(5):1188-95
pubmed: 23418397
J Cell Sci. 1997 Nov;110 ( Pt 21):2661-71
pubmed: 9427384
R Soc Open Sci. 2017 May 3;4(5):170095
pubmed: 28573017