Symbiont community complexity and dynamics. Cameron Currie Department of Bacteriology University of Wisconsin-Madison

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1 Symbiont community complexity and dynamics Cameron Currie Department of Bacteriology University of Wisconsin-Madison

2 Acknowledgements Current Lab Members Collaborators Funding NIH NSF DOE-GLBRC USDA JGI Frank Aylward Adam Book Eric Caldera Kirk Grubbs Alissa Hanshew Heidi Horn Jonathan Klassen Gina Lewin Sarah Marsh Bradon McDonald Joe Moeller Laura Schwab Past lab members Jarrod Scott Garret Suen Matias Cafaro Jiri Hulcr Ainslie Little Adrian Pinto Michael Poulsen Rebeccah Steffensen Patrick Abbot Aaron Adams David Andes Teri Balser Kerrie Barry Peter Biedermann Johan Billen Koos Boomsma David Bruce Tim Bugni Kristin Burnum Amy Cavanaugh Jon Clardy Sandra Clifton Tim Donahue Michael Fischbach Brian Fox Jeremy Glasner Nicole Gerardo Lynne Goodwin Michael Hoffman Bruce Klein Kier Klepzig Julia Kubanek Lewyn Li Mary Lipton Dong-Chan Oh Nicole Perna Ken Raffa Ted Schultz David Schwartz Steve Slater Clotilde Teiling Michael Thomas Susannah Tringe Paul Weimer George Weinstock Shiguo Zhou

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5 Agriculture in ants J. Høeg Benefit to fungus Dispersal Substrate for growth Protection Benefit to the ants Fungus serves as main food source for larvae and queen Obligate mutualism, origin ~45 mya

6 Fungus farms infected by specialized pathogens - Microfungi in the genus Escovopsis - Specialized and potentially virulent pathogen of the fungus garden - Secretes enzymes that break-down the cultivar - Forms persistent infections that impact colony fitness (Currie et al PNAS, Currie 2001a Oecologia, Reynolds and Currie 2004)

7 Wax on the ants is actinobacteria A. Little

8 Chemical defense of the fungus garden Genus Pseudonocardia (Actinobacteria) Visible on workers across most of the phylogenetic diversity of fungus-growing ants Vertical transmitted from parent to offspring nest Produces small molecules that inhibit Escovopsis (Currie et al Nature)

9 Evidence for actinobacteria involved in garden defense 1. 3 separate in vivo experiments 2. More abundant on garden tending workers 3. Increase in abundance under experimental infection 4. Natural product chemistry (a cyclic depsipeptide) (Oh et al Nature Chem. Bio) Dong-Chan Oh Jon Clardy

10 Outline Evidence that the use of antibioticproducing bacteria is ancient in ants and that it is a highly specialized relationship Evidence that the use of antibioticproducing bacteria is widespread in insects Insights into microbial community dynamics Importance of context dependence Stability through complexity? Further complexity

11 Is the use of antibiotic-producing bacteria ancient? A. Little Cyphomyrmex longiscapus Alex Wild

12 Is the use of antibiotic-producing bacteria ancient?

13 Dominican Amber (Currie et al. in prep)

14 Acquisition of Actinobacteria Pupae 1 day old adult 6 day old adult Full coverage 14+ day old adult

15 Acquisition of Pseudonocardia Pupae Pupae + + Atta Minor 3. + Pupae Major without Pseudo Pupae Major with Pseudo.

16 Proportion of ants acquiring Pseudonocardia Pseudonocardia Acquisition Sarah Marsh 100% 90% 80% 70% 60% 50% 40% 30% 20% 10% Acquired Pseudonocardia No Pseudonocardia 0% n = 14 n = 7 n = 7 n = 7 Atta raised minor raised Pseudonocardia-free major raised Major raised

17 Acquisition of Actinobacteria Add major with Pseudonocardia Pupae + Minor Major without Pseudonocardia hours post eclosion hours post eclosion hours post eclosion hours post eclosion????

18 Percent acquiring Pseudonocardia Acquisition of Pseudonocardia Sarah Marsh 100% Acquired Clear n = 9 n = 11 n = 9 n = 3 n = 10 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Control 0-1 hour 1-2 hours 7-8 hours 24 hours Time

19 Part 2: Is the use of antibiotic-producing bacteria widespread? Beneficial fungus Entomocorticium sp. Antagonistic fungus Ophiostoma minus

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21 (Scott et al. 2008, Science) (Collaboration with Oh and Clardy, Harvard University)

22 The honey bee antagonistic P. larvae symbiotic bacteria (actinomycete)

23 Novel small molecule apinimycin with high specificity towards P. larvae 48 nm 213 nm 6 μm Renee Kontnik, (Clardy lab, Harvard)

24 Insect-symbiotic actinobacteria as a source of natural products HO N N HN O O O NH N HN N O HN OH A. Little O HO O HN O O O OH - In collaboration with Clardy-lab, we have discovered 4 other unpublished novel small molecules

25 Part 3a: Context dependence, black yeast symbionts Dr. Ainslie Little

26 Black yeast: Context dependence Apterostigma colony Black yeast + - Escovopsis ANOVA, d.f. = 43, F = , P < 0.001

27 Part 3b: Stability through community interactions Cultivar Ants - - Crossed presence/absence of cheating by the ants with presence/absence of garden infection - Cheating by ants involved increased production of males Garden parasite

28 Part 3b: Stability through community interactions

29 Summary Evidence that the use of antibioticproducing bacteria is ancient in ants and that it is a highly specialized relationship Evidence that the use of antibioticproducing bacteria is widespread in insec Jake McKinlay Insights into microbial community dynamics Importance of context dependence Stability through complexity?