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Comparative Study
. 2011;6(5):e19055.
doi: 10.1371/journal.pone.0019055. Epub 2011 May 13.

A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans

Ilka Engelmann  1 , Aurélien Griffon, Laurent Tichit, Frédéric Montañana-Sanchis, Guilin Wang, Valerie Reinke, Robert H Waterston, LaDeana W Hillier, Jonathan J Ewbank
Affiliations
Comparative Study

A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans

Ilka Engelmann et al. PLoS One. 2011.

Abstract

While Caenorhabditis elegans specifically responds to infection by the up-regulation of certain genes, distinct pathogens trigger the expression of a common set of genes. We applied new methods to conduct a comprehensive and comparative study of the transcriptional response of C. elegans to bacterial and fungal infection. Using tiling arrays and/or RNA-sequencing, we have characterized the genome-wide transcriptional changes that underlie the host's response to infection by three bacterial (Serratia marcescens, Enterococcus faecalis and otorhabdus luminescens) and two fungal pathogens (Drechmeria coniospora and Harposporium sp.). We developed a flexible tool, the WormBase Converter (available at http://wormbasemanager.sourceforge.net/), to allow cross-study comparisons. The new data sets provided more extensive lists of differentially regulated genes than previous studies. Annotation analysis confirmed that genes commonly up-regulated by bacterial infections are related to stress responses. We found substantial overlaps between the genes regulated upon intestinal infection by the bacterial pathogens and Harposporium, and between those regulated by Harposporium and D. coniospora, which infects the epidermis. Among the fungus-regulated genes, there was a significant bias towards genes that are evolving rapidly and potentially encode small proteins. The results obtained using new methods reveal that the response to infection in C. elegans is determined by the nature of the pathogen, the site of infection and the physiological imbalance provoked by infection. They form the basis for future functional dissection of innate immune signaling. Finally, we also propose alternative methods to identify differentially regulated genes that take into account the greater variability in lowly expressed genes.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Genes regulated by bacterial infection.
Proportional Venn diagrams showing the overlap of genes up-(A) or down-regulated (B) by S. marcescens, E. faecalis, P. luminescens using RNA-seq.
Figure 2
Figure 2. Genes regulated by fungal or bacterial infection.
Proportional Venn diagrams showing the overlap of genes up-(A) or down-regulated (B) by Harposporium sp., D. coniospora and three bacteria (common to S. marcescens, E. faecalis and P. luminescens) using RNA-seq. The asterisk indicates that 11 genes were up-regulated by Harposporium sp., D. coniospora and three bacteria; 6 genes were down-regulated by the three bacteria and either Harposporium sp. or D. coniospora.
Figure 3
Figure 3. Peptide length of induced transcripts.
Transcripts up-regulated upon fungal infection are on average shorter than those induced by bacterial infection. All transcripts were divided into five classes based on the length of the encoded proteins as shown (AA: amino acid). Bar diagram showing the percentages of transcripts coding for proteins with a certain length in the list of all transcripts and in the lists of up-regulated transcripts for different pathogens (RNA-seq). All: all transcripts; Dc: D. coniospora; Har: Harposporium sp.; Sm: S. marcescens; Ef: E. faecalis; Pl: P. luminescens.
Figure 4
Figure 4. The WormBase Converter.
Constant changes in gene annotations create the need for WormBase Converter. (A) Example of the gene R07E5.12 that has undergone a merge with R07E5.10, which then has been re-annotated. More recently, as seen here in WS220, the structure of R07E5.10 has been further modified. (B) Example of an input list with CDS Sequence names as identifiers based on WormBase version WS150 and the corresponding output list in WS210 using gene sequence name as identifier. The output list can be copied and pasted into any spreadsheet for further use. The number of successfully converted genes is indicated. In this case, 11 out of 413 genes were absent from the output list; 5 had been “killed”, and 6 not found in the WS150 release. On the other hand, because of gene splits, the output list contained 4 new genes. (C) List showing the changes that occurred during the conversions, the nature of the change and the version when the change was implemented, including the 5 “killed” genes. (D) List of 6 genes that were not found in the version used as input.
Figure 5
Figure 5. Selection of differentially-regulated transcripts.
Dot plots showing log10 transformed dcpm values for expression of transcripts in uninfected (x-axis) versus D. coniospora infected worms (y-axis). Transcripts identified as up-regulated by one or more methods are shown in black, the others are shown in grey. (A) transcripts defined as up-regulated if the log2 fold change is greater than the 97th percentile of all up-regulated transcripts; (B) transcripts defined as up-regulated by alternative approach 1 (see Methods); (C) transcripts defined as up-regulated by alternative approach 2 (see Methods); (D) transcripts only defined as up-regulated if the log2 fold change is greater than the 97th percentile of all up-regulated transcripts and not by either of the other methods; (E) transcripts only defined as up-regulated by alternative approach 1; (F) transcripts only defined as up-regulated by alternative approach 2.
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