Establishment of Host-Algal Endosymbioses: Genetic Response to Symbiont Versus Prey in a Sponge Host.


Journal

Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707

Informations de publication

Date de publication:
05 11 2021
Historique:
accepted: 08 11 2021
pubmed: 19 11 2021
medline: 1 4 2022
entrez: 18 11 2021
Statut: ppublish

Résumé

The freshwater sponge Ephydatia muelleri and its Chlorella-like algal partner is an emerging model for studying animal: algal endosymbiosis. The sponge host is a tractable laboratory organism, and the symbiotic algae are easily cultured. We took advantage of these traits to interrogate questions about mechanisms that govern the establishment of durable intracellular partnerships between hosts and symbionts in facultative symbioses. We modified a classical experimental approach to discern the phagocytotic mechanisms that might be co-opted to permit persistent infections, and identified genes differentially expressed in sponges early in the establishment of endosymbiosis. We exposed algal-free E. muelleri to live native algal symbionts and potential food items (bacteria and native heat-killed algae), and performed RNA-Seq to compare patterns of gene expression among treatments. We found a relatively small but interesting suite of genes that are differentially expressed in the host exposed to live algal symbionts, and a larger number of genes triggered by host exposure to heat-killed algae. The upregulated genes in sponges exposed to live algal symbionts were mostly involved in endocytosis, ion transport, metabolic processes, vesicle-mediated transport, and oxidation-reduction. One of the host genes, an ATP-Binding Cassette transporter that is downregulated in response to live algal symbionts, was further evaluated for its possible role in the establishment of the symbiosis. We discuss the gene expression profiles associated with host responses to living algal cells in the context of conditions necessary for long-term residency within host cells by phototrophic symbionts as well as the genetic responses to sponge phagocytosis and immune-driven pathways.

Identifiants

pubmed: 34791195
pii: 6427630
doi: 10.1093/gbe/evab252
pmc: PMC8633732
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : P20 GM103423
Pays : United States

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Références

Eukaryot Cell. 2013 Feb;12(2):265-77
pubmed: 23243063
Nucleic Acids Res. 2021 Jan 8;49(D1):D480-D489
pubmed: 33237286
Philos Trans R Soc Lond B Biol Sci. 2010 Mar 12;365(1541):699-712
pubmed: 20124339
Protoplasma. 2007;230(1-2):61-7
pubmed: 17111098
Infect Immun. 2008 Nov;76(11):4905-12
pubmed: 18765732
Trends Biochem Sci. 2018 Jun;43(6):412-423
pubmed: 29636212
Hum Genomics. 2009 Apr;3(3):281-90
pubmed: 19403462
Curr Biol. 2018 Aug 20;28(16):2570-2580.e6
pubmed: 30100341
J Surg Res. 2006 Nov;136(1):58-69
pubmed: 16979664
J Phycol. 2017 Oct;53(5):951-960
pubmed: 28796903
Science. 1996 Jan 19;271(5247):363-6
pubmed: 8553074
Cell Biochem Funct. 2020 Jul;38(5):533-540
pubmed: 32207552
Cell Commun Signal. 2020 Nov 25;18(1):186
pubmed: 33239048
Genome Biol. 2002 Jun 18;3(7):RESEARCH0034
pubmed: 12184808
Microbiol Mol Biol Rev. 2007 Jun;71(2):295-347
pubmed: 17554047
J Exp Biol. 2008 Oct;211(Pt 19):3059-66
pubmed: 18805804
Mol Phylogenet Evol. 2011 Apr;59(1):81-8
pubmed: 21256238
Adv Biol Regul. 2016 Sep;62:37-49
pubmed: 27220739
J Hepatol. 2001 Dec;35(6):765-73
pubmed: 11738104
J Cell Sci. 2009 Nov 15;122(Pt 22):4081-8
pubmed: 19843583
G3 (Bethesda). 2019 Jul 9;9(7):2337-2347
pubmed: 31097480
Immunol Rev. 2007 Oct;219:143-56
pubmed: 17850487
Mol Biol Evol. 2020 Dec 16;37(12):3485-3506
pubmed: 32929503
Nucleic Acids Res. 2012 May;40(10):4288-97
pubmed: 22287627
Nucleic Acids Res. 2007 Jan;35(Database issue):D61-5
pubmed: 17130148
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Proc Natl Acad Sci U S A. 1958 Dec 15;44(12):1259-63
pubmed: 16590343
Front Microbiol. 2014 Jul 17;5:357
pubmed: 25101064
J Lipid Res. 2001 Jul;42(7):1007-17
pubmed: 11441126
Cell Death Differ. 1998 Jul;5(7):563-8
pubmed: 10200510
Biol Bull. 2010 Dec;219(3):189-97
pubmed: 21183440
Protoplasma. 2011 Apr;248(2):325-37
pubmed: 20582727
Front Immunol. 2016 Apr 25;7:159
pubmed: 27199984
Philos Trans R Soc Lond B Biol Sci. 2009 Jan 12;364(1513):85-98
pubmed: 18930879
Molecules. 2018 Aug 23;23(9):
pubmed: 30142934
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Curr Pharm Biotechnol. 2011 Apr;12(4):621-35
pubmed: 21118091
Nucleic Acids Res. 2008 Jun;36(10):3420-35
pubmed: 18445632
Sci Rep. 2017 Sep 28;7(1):12389
pubmed: 28959041
Front Immunol. 2021 Jun 16;12:689051
pubmed: 34220847
Microbiol Mol Biol Rev. 2012 Jun;76(2):229-61
pubmed: 22688813
Front Immunol. 2019 May 14;10:1069
pubmed: 31139191
Front Immunol. 2019 Jul 04;10:1473
pubmed: 31333644
Molecules. 2018 Nov 01;23(11):
pubmed: 30388847
J Biol Chem. 2008 Apr 18;283(16):11004-13
pubmed: 18263583
BMC Genomics. 2014 Nov 18;15:993
pubmed: 25407996
Bioinformatics. 2017 Nov 15;33(22):3635-3637
pubmed: 29036533
Front Cell Dev Biol. 2015 Oct 26;3:66
pubmed: 26579519
Biochem Biophys Res Commun. 1999 Feb 5;255(1):143-9
pubmed: 10082670
J Exp Biol. 2003 Sep;206(Pt 18):3149-57
pubmed: 12909696
Elife. 2018 May 31;7:
pubmed: 29848439
Genome Biol. 2007;8(2):R19
pubmed: 17291332
Microbiologyopen. 2018 Oct;7(5):e00632
pubmed: 29692003
Integr Comp Biol. 2019 Oct 1;59(4):845-855
pubmed: 31150064
Nat Rev Mol Cell Biol. 2009 Mar;10(3):218-27
pubmed: 19234479
Cell Rep. 2016 Nov 1;17(6):1518-1531
pubmed: 27806292
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Mol Cell Biol. 2004 May;24(10):4593-604
pubmed: 15121875
Immunity. 2005 Jan;22(1):9-18
pubmed: 15664155
PeerJ. 2021 Feb 11;9:e10654
pubmed: 33614268
BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Nat Rev Immunol. 2003 Oct;3(10):791-800
pubmed: 14502271
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
J Cell Sci. 2005 Sep 1;118(Pt 17):4039-48
pubmed: 16129887
Protoplasma. 2007;231(1-2):55-63
pubmed: 17602279
Nat Cell Biol. 2008 Oct;10(10):1135-45
pubmed: 18794847
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Bioinformatics. 2005 Sep 15;21(18):3674-6
pubmed: 16081474
PLoS One. 2011;6(10):e26687
pubmed: 22039532
Int J Mol Sci. 2018 May 25;19(6):
pubmed: 29799467
FASEB J. 2014 Jan;28(1):162-75
pubmed: 24036885
J Exp Bot. 2008;59(5):1069-80
pubmed: 18267943
BMC Genomics. 2014 Mar 10;15:183
pubmed: 24612690
Front Immunol. 2012 Jun 01;3:140
pubmed: 22675327
J Cell Sci. 2018 Nov 5;131(21):
pubmed: 30397181
Biol Rev Camb Philos Soc. 2012 Nov;87(4):804-21
pubmed: 22404964
Mol Syst Biol. 2010 Oct 19;6:423
pubmed: 20959821
Genes (Basel). 2021 Jan 11;12(1):
pubmed: 33440651
Br J Cancer. 1972 Aug;26(4):239-57
pubmed: 4561027
Genome Res. 2007 Mar;17(3):377-86
pubmed: 17255551
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
pubmed: 9254694
Mol Phylogenet Evol. 2016 Oct;103:19-25
pubmed: 27404042
Proc Natl Acad Sci U S A. 2021 Sep 21;118(38):
pubmed: 34521754
Nat Commun. 2020 Jul 27;11(1):3676
pubmed: 32719321
Biochim Biophys Acta Mol Cell Res. 2019 May;1866(5):916-929
pubmed: 30771381
Plant Cell. 2010 May;22(5):1483-97
pubmed: 20453115
Protoplasma. 2005 Oct;225(3-4):191-203
pubmed: 15997335
Cell. 1999 Jan 22;96(2):245-54
pubmed: 9988219

Auteurs

Sara Geraghty (S)

Department of Biology, University of Richmond, Virginia, USA.
Lewis-Sigler Institute for Integrative Genomics, Princeton University, New Jersey, USA.

Vasiliki Koutsouveli (V)

Department of Life Sciences, Natural History Museum, London, United Kingdom.
Department of Marine Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.

Chelsea Hall (C)

Department of Biology, University of Richmond, Virginia, USA.
Department of Microbiology, Immunology, and Cancer Biology, University of Virginia, Charlottesville, Virginia, USA.

Lillian Chang (L)

Department of Biology, Bates College, Lewiston, Maine, USA.

Oriol Sacristan-Soriano (O)

Department of Biology, University of Richmond, Virginia, USA.
Centro de Estudios Avanzados de Blanes (CEAB, CSIC), Blanes, Spain.

Malcolm Hill (M)

Department of Biology, University of Richmond, Virginia, USA.
Department of Biology, Bates College, Lewiston, Maine, USA.

Ana Riesgo (A)

Department of Life Sciences, Natural History Museum, London, United Kingdom.
Department of Biodiversity and Evolutionary Biology, National Museum of Natural Sciences, Madrid, Spain.

April Hill (A)

Department of Biology, University of Richmond, Virginia, USA.
Department of Biology, Bates College, Lewiston, Maine, USA.

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Classifications MeSH