title: Specificity and stability of the Acromyrmex-Pseudonocardia symbiosis.
abstract: The stability of mutualistic interactions is likely to be affected by the genetic diversity of symbionts that compete for the same functional niche. Fungus-growing (attine) ants have multiple complex symbioses and thus provide ample opportunities to address questions of symbiont specificity and diversity. Among the partners are Actinobacteria of the genus Pseudonocardia that are maintained on the ant cuticle to produce antibiotics, primarily against a fungal parasite of the mutualistic gardens. The symbiosis has been assumed to be a hallmark of evolutionary stability, but this notion has been challenged by culturing and sequencing data indicating an unpredictably high diversity. We used 454 pyrosequencing of 16S rRNA to estimate the diversity of the cuticular bacterial community of the leaf-cutting ant Acromyrmex echinatior and other fungus-growing ants from Gamboa, Panama. Both field and laboratory samples of the same colonies were collected, the latter after colonies had been kept under laboratory conditions for up to 10 years. We show that bacterial communities are highly colony-specific and stable over time. The majority of colonies (25/26) had a single dominant Pseudonocardia strain, and only two strains were found in the Gamboa population across 17 years, confirming an earlier study. The microbial community on newly hatched ants consisted almost exclusively of a single strain of Pseudonocardia while other Actinobacteria were identified on older, foraging ants in varying but usually much lower abundances. These findings are consistent with recent theory predicting that mixtures of antibiotic-producing bacteria can remain mutualistic when dominated by a single vertically transmitted and resource-demanding strain.
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, 2100, Copenhagen, Denmark.
authors.forename: S B
authors.initials: SB
authors.lastname: Andersen
authors.affiliation: Molecular Microbial Ecology Group, Department of Biology, University of Copenhagen, 2100, Copenhagen, Denmark.
authors.forename: L H
authors.initials: LH
authors.lastname: Hansen
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, 2100, Copenhagen, Denmark.
authors.forename: P
authors.initials: P
authors.lastname: Sapountzis
authors.affiliation: Molecular Microbial Ecology Group, Department of Biology, University of Copenhagen, 2100, Copenhagen, Denmark.
authors.forename: S J
authors.initials: SJ
authors.lastname: Sørensen
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, 2100, Copenhagen, Denmark.
authors.forename: J J
authors.initials: JJ
authors.lastname: Boomsma
mesh_terms: D000192:Actinomycetales / Q000145:classification* / Q000235:genetics*; D000818:Animals; D001000:Ants / Q000235:genetics / Q000382:microbiology*; D014644:Genetic Variation; D010176:Panama; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017422:Sequence Analysis, DNA / Q000379:methods; D013045:Species Specificity; D013559:Symbiosis
chemical_list: D012336:RNA, Ribosomal, 16S
keywords: 454 pyrosequencing; Pseudonocardia; attine ant mutualism; bacterial community
references.citation: Q Rev Biol. 1996 Mar;71(1):37-78
references.pmid: 8919665
references.citation: Proc Biol Sci. 2009 Jun 22;276(1665):2263-9
references.pmid: 19324734
references.citation: J Clin Microbiol. 2002 Nov;40(11):4211-7
references.pmid: 12409400
references.citation: Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7998-8002
references.pmid: 10393936
references.citation: Nature. 2010 Mar 4;464(7285):59-65
references.pmid: 20203603
references.citation: Evolution. 2001 Oct;55(10):1980-91
references.pmid: 11761059
references.citation: Evolution. 2011 Jun;65(6):1791-9
references.pmid: 21644963
references.citation: Am Nat. 2012 Nov;180(5):604-17
references.pmid: 23070321
references.citation: J Evol Biol. 2012 Jul;25(7):1340-50
references.pmid: 22530696
references.citation: Ecol Lett. 2011 Dec;14(12):1300-12
references.pmid: 22011186
references.citation: Proc Biol Sci. 2011 Jun 22;278(1713):1814-22
references.pmid: 21106596
references.citation: Am Nat. 2011 Jan;177(1):75-85
references.pmid: 21091210
references.citation: Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17611-2
references.pmid: 19826091
references.citation: Mol Ecol. 2005 Oct;14(11):3597-604
references.pmid: 16156826
references.citation: Science. 2010 Oct 8;330(6001):243-6
references.pmid: 20929776
references.citation: PLoS One. 2012;7(10):e46231
references.pmid: 23056268
references.citation: Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21236-41
references.pmid: 19948964
references.citation: Evolution. 2008 Nov;62(11):2894-912
references.pmid: 18752608
references.citation: Appl Environ Microbiol. 2009 Dec;75(23):7537-41
references.pmid: 19801464
references.citation: Proc Biol Sci. 2001 May 22;268(1471):1033-9
references.pmid: 11375087
references.citation: Trends Ecol Evol. 1999 Feb;14(2):49-53
references.pmid: 10234251
references.citation: PLoS Biol. 2012;10(11):e1001424
references.pmid: 23185130
references.citation: PLoS One. 2010 Sep 10;5(9):
references.pmid: 20844760
references.citation: Environ Microbiol Rep. 2010 Aug;2(4):534-540
references.pmid: 22896766
references.citation: BMC Evol Biol. 2002 May 03;2:9
references.pmid: 12019020
references.citation: Naturwissenschaften. 2003 Sep;90(9):406-9
references.pmid: 14504783
references.citation: Proc Natl Acad Sci U S A. 2009 Mar 24;106(12):4742-6
references.pmid: 19270078
references.citation: PLoS One. 2011;6(8):e22028
references.pmid: 21857911
references.citation: Biol Lett. 2012 Jun 23;8(3):461-4
references.pmid: 22130174
references.citation: Nature. 2003 Sep 4;425(6953):78-81
references.pmid: 12955144
references.citation: Antonie Van Leeuwenhoek. 2010 Aug;98(2):195-212
references.pmid: 20333466
references.citation: Naturwissenschaften. 2007 Oct;94(10):821-8
references.pmid: 17541536
references.citation: Science. 2003 Jan 17;299(5605):386-8
references.pmid: 12532015
references.citation: Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17805-10
references.pmid: 19805175
references.citation: Ecol Lett. 2012 Nov;15(11):1300-1307
references.pmid: 22913725
references.citation: Proc Natl Acad Sci U S A. 2008 Apr 8;105(14):5435-40
references.pmid: 18362345
references.citation: Science. 2005 Feb 4;307(5710):741-4
references.pmid: 15692054
references.citation: Science. 2009 Nov 20;326(5956):1103-6
references.pmid: 19965427
references.citation: Science. 2006 Jan 6;311(5757):81-3
references.pmid: 16400148
references.citation: Am Nat. 2003 Oct;162(4 Suppl):S51-62
references.pmid: 14583857
references.citation: Int J Syst Bacteriol. 1999 Jan;49 Pt 1:149-62
references.pmid: 10028256
references.citation: Sci Rep. 2011;1:204
references.pmid: 22355719
references.citation: BMC Biol. 2010 Aug 26;8:109
references.pmid: 20796277
references.citation: Commun Integr Biol. 2011 Jan;4(1):41-3
references.pmid: 21509175
references.citation: Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1955-60
references.pmid: 21245311
references.citation: Can J Microbiol. 2005 Jun;51(6):441-6
references.pmid: 16121221
references.citation: PLoS Biol. 2006 Jul;4(8):e235
references.pmid: 16805647