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Can't Take the Heat: High Temperature Depletes Bacterial Endosymbionts of Ants

  • Host Microbe Interactions
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Abstract

Members of the ant tribe Camponotini have coevolved with Blochmannia, an obligate intracellular bacterial mutualist. This endosymbiont lives within host bacteriocyte cells that line the ant midgut, undergoes maternal transmission from host queens to offspring, and contributes to host nutrition via nitrogen recycling and nutrient biosynthesis. While elevated temperature has been shown to disrupt obligate bacterial mutualists of some insects, its impact on the ant-Blochmannia partnership is less clear. Here, we test the effect of heat on the density of Blochmannia in two related Camponotus species in the lab. Transcriptionally active Blochmannia were quantified using RT-qPCR as the ratio of Blochmannia 16S rRNA to ant host elongation factor 1-α transcripts. Our results showed that 4 weeks of heat treatment depleted active Blochmannia by >99 % in minor workers and unmated queens. However, complete elimination of Blochmannia transcripts rarely occurred, even after 16 weeks of heat treatment. Possible mechanisms of observed thermal sensitivity may include extreme AT-richness and related features of Blochmannia genomes, as well as host stress responses. Broadly, the observed depletion of an essential microbial mutualist in heat-treated ants is analogous to the loss of zooanthellae during coral bleaching. While the ecological relevance of Blochmannia's thermal sensitivity is uncertain, our results argue that symbiont dynamics should be part of models predicting how ants and other animals will respond and adapt to a warming climate.

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References

  1. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  Google Scholar 

  2. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, Inc, New York

    Google Scholar 

  3. Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474

    Article  Google Scholar 

  4. Wernegreen JJ (2012) Mutualism meltdown in insects: bacteria constrain thermal adaptation. Curr Opin Microbiol 22(14):R555–R561

    CAS  Google Scholar 

  5. Ohtaka C, Ishikawa H (1991) Effects of heat treatment on the symbiotic system of an aphid mycetocyte. Symbiosis 11:19–30

    Google Scholar 

  6. Montllor C, Maxmen A, Purcell A (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  7. Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci U S A 96:6814–6819

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Sacchi L, Grigolo A, Biscaldi G, Laudani U (1993) Effects of heat treatment on the symbiotic system of Blattoidea: morphofunctional alterations of bacteriocytes. Ital J Zool 60:271–279

    Google Scholar 

  9. Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci 273:603–610

    Article  PubMed Central  PubMed  Google Scholar 

  10. Bolton B (1995) A new general catalogue of the ants of the world. Harvard University Press, Cambridge, MA, 504 pp

    Google Scholar 

  11. Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, Latorre A, Rausell C, Kamerbeek J, Gadau J, Holldobler B, van Ham RC, Gross R, Moya A (2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci U S A 100:9388–9393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Degnan PH, Lazarus AB, Wernegreen JJ (2005) Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res 15:1023–1033

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Williams LE, Wernegreen JJ (2010) Unprecedented loss of ammonia assimilation capability in a urease-encoding bacterial mutualist. BMC Genomics 11:687

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S, Mueller MJ, Gross R (2007) Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 5:48

    Article  PubMed Central  PubMed  Google Scholar 

  15. de Souza DJ, Bezier A, Depoix D, Drezen JM, Lenoir A (2009) Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah. BMC Microbiol 9:29

    Article  PubMed Central  PubMed  Google Scholar 

  16. Sauer C, Dudaczek D, Holldobler B, Gross R (2002) Tissue localization of the endosymbiotic bacterium “Candidatus Blochmannia floridanus” in adults and larvae of the carpenter ant Camponotus floridanus. Appl Environ Microbiol 68:4187–4193

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Wernegreen JJ, Kauppinen SN, Brady SG, Ward PS (2009) One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects. BMC Evol Biol 9:292

    Article  PubMed Central  PubMed  Google Scholar 

  18. Bhatkar A, WW H (1971) Artificial diet for rearing various species of ants. Fla Entomol 53:229–232

    Article  Google Scholar 

  19. Chen CY, Lai CY, Kuo MH (2009) Temperature effect on the growth of Buchnera endosymbiont in Aphis craccivora (Hemiptera: Aphididae). Symbiosis 49:53–59

    Article  Google Scholar 

  20. J-s K, Wang N (2009) Characterization of copy numbers of 16S rDNA and 16S rRNA of Candidatus Liberibacter asiaticus and the implication in detection in plants using quantitative PCR. BMC Res Notes 2:37

    Article  Google Scholar 

  21. Bronikowski AM, Bennett AF, Lenski RE (2001) Evolutionary adaptation to temperature. VIII. Effects of temperature on growth rate in natural isolates of Escherichia coli and Salmonella enterica from different thermal environments. Evolution 55:33–40

    Article  CAS  PubMed  Google Scholar 

  22. McCutcheon JP, Moran NA (2011) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10(1):13–26

    PubMed  Google Scholar 

  23. Yakovchuk P, Protozanova E, Frank-Kamenetskii MD (2006) Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res 34:564–574

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Moran NA (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 93:2873–2878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernandez JM, Jimenez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Moran F, Moya A (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100:581–586

    Article  PubMed Central  PubMed  Google Scholar 

  26. Heddi A, Charles H, Khatchadourian C, Bonnot G, Nardon P (1998) Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar G + C content of an endocytobiotic DNA. J Mol Evol 47:52–61

    Article  CAS  PubMed  Google Scholar 

  27. Wilcox JL, Dunbar HE, Wolfinger RD, Moran NA (2003) Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol Microbiol 48(6):1491–1500

    Article  CAS  PubMed  Google Scholar 

  28. Stoll S, Feldhaar H, Gross R (2009) Transcriptional profiling of the endosymbiont Blochmannia floridanus during different developmental stages of its holometabolous ant host. Environ Microbiol 11:877–888

    Article  CAS  PubMed  Google Scholar 

  29. Hölldobler B, Wilson EO (1990) The Ants. Belknap Press of Harvard University Press, Cambridge

    Book  Google Scholar 

  30. Mueller UG, Mikheyev AS, Hong EK, Sen R, Warren DL, Solomon SE, Ishak HD, Cooper M, Miller JL, Shaffer KA, Juenger TE (2011) Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis. Proc Natl Acad Sci U S A 108:4053–4056

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Dunbar HE, Wilson AC, Ferguson NR, Moran NA (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5:e96

    Article  PubMed Central  PubMed  Google Scholar 

  32. Harmon JP, Moran NA, Ives AR (2009) Species response to environmental change: impacts of food web interactions and evolution. Science 323:1347–1350

    Article  CAS  PubMed  Google Scholar 

  33. Burke GR, McLaughlin HJ, Simon JC, Moran NA (2010) Dynamics of a recurrent Buchnera mutation that affects thermal tolerance of pea aphid hosts. Genetics 186:367–372

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

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Acknowledgment

We thank Adam B. Lazarus for performing the MBL temperature experiments. We are grateful to Tatiana Fofanova and Bryan P. Brown for their help with NC ant collection and rearing. We thank Diana E. Wheeler for helpful discussion of temperature effects on endosymbionts. We appreciate the comments of four anonymous reviewers. Funding was provided by grants from the NSF (MCB-1103113) and NIH (R01GM062626) to JJW.

Author information

Authors and Affiliations

  1. Institute for Genome Sciences and Policy, Duke University, Durham, NC, USA

    Yongliang Fan & Jennifer J. Wernegreen

  2. Nicholas School of the Environment, Duke University, Durham, NC, USA

    Jennifer J. Wernegreen

  3. CIEMAS, Rm. 2175, Box 3382, 101 Science Dr, Durham, NC, USA

    Jennifer J. Wernegreen

Authors
  1. Yongliang Fan
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  2. Jennifer J. Wernegreen
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Corresponding author

Correspondence to Jennifer J. Wernegreen.

Additional information

Some portions of the Introduction and Discussion previously appeared in ref. 4.

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Supplemental Table 1

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Supplementary Fig. 1

Copy numbers of Blochmannia 16S rRNA, not host EF1α, varied due to heat treatment. Data show absolute copy numbers of 16S rRNA and host EF1α transcripts for the final sample of each experiment (t = 4 or t = 16). Heat-treated samples are outlined in yellow. Absolute copy number of 16S rRNA declined under heat treatment, but absolute copy number of host EF1α transcripts was more consistent across treatments. The right-most group on the x-axis shows data for worker heads, used as negative controls in this study. See figures in main text for sample sizes. a Bars show mean absolute copy numbers ± standard error. b Individual data points underlying the mean values presented in (a). Each point represents the copy number of 16S rRNA or EF1α transcripts in a single ant gaster (or dissected tissue from one gaster), calculated as the average of three RT-qPCR triplicates for that single sample. W, whole gaster of minor worker; Wg, dissected worker midgut; Wr, rest of the worker gaster (excluding midgut); Qg, dissected queen midgut; Qo, dissected queen ovary. (PDF 123 kb)

Supplementary Fig. 2

Heat treatment of Camponotus chromaiodes depleted, but usually did not eliminate, Blochmannia. Chart shows individual data points underlying the mean values represented in Figs. 3 and 4 of the main text. Heat-treated samples are outlined in yellow. Horizontal reference line marks the highest ratio detected in negative controls (worker heads, right-most group on x-axis). The lower ratio under heat treatment reflects the depletion of Blochmannia from whole gasters. However, values for just one whole worker gaster and one dissected worker midgut fell within the range of worker heads used as negative controls, suggesting that Blochmannia was eliminated only rarely. Comparisons of dissected worker midguts versus the rest of the gaster indicate that midguts harbor the vast majority of Blochmannia. W, whole gaster of minor worker; Wg, dissected worker midgut; Wr, rest of the worker gaster (excluding midgut). (PDF 123 kb)

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Fan, Y., Wernegreen, J.J. Can't Take the Heat: High Temperature Depletes Bacterial Endosymbionts of Ants. Microb Ecol 66, 727–733 (2013). https://doi.org/10.1007/s00248-013-0264-6

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