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Microbial Ecology

, Volume 66, Issue 3, pp 727–733 | Cite as

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

  • Yongliang Fan
  • Jennifer J. Wernegreen
Host Microbe Interactions

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.

Keywords

Minor Worker rRNA Transcript Electronic Supplementary Material Supplementary Absolute Copy Number Female Alate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

Supplementary material

248_2013_264_MOESM1_ESM.pdf (64 kb)
Supplemental Table 1 (PDF 63 kb)
248_2013_264_MOESM2_ESM.pdf (123 kb)
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)
248_2013_264_MOESM2_ESM.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)
248_2013_264_MOESM3_ESM.pdf (73 kb)
ESM 3 (PDF 73.1 kb)

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Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Institute for Genome Sciences and PolicyDuke UniversityDurhamUSA
  2. 2.Nicholas School of the EnvironmentDuke UniversityDurhamUSA
  3. 3.DurhamUSA

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