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Microbial Ecology

, Volume 78, Issue 3, pp 618–630 | Cite as

Enhanced Growth of Pilin-Deficient Geobacter sulfurreducens Mutants in Carbon Poor and Electron Donor Limiting Conditions

  • Lucie Semenec
  • Ismael A. Vergara
  • Andrew E. Laloo
  • Elizabeth R. Mathews
  • Philip L. Bond
  • Ashley E. FranksEmail author
Environmental Microbiology

Abstract

Geobacter sulfurreducens pili enable extracellular electron transfer and play a role in secretion of c-type cytochromes such as OmcZ. PilA-deficient mutants of G. sulfurreducens have previously been shown to accumulate cytochromes within their membranes. This cytochrome retaining phenotype allowed for enhanced growth of PilA-deficient mutants in electron donor and carbon-limited conditions where formate and fumarate are provided as the sole electron donor and acceptor with no supplementary carbon source. Conversely, wild-type G. sulfurreducens, which has normal secretion of cytochromes, has comparative limited growth in these conditions. This growth is further impeded for OmcZ-deficient and OmcS-deficient mutants. A PilB-deficient mutant which prevents pilin production but allows for secretion of OmcZ had moderate growth in these conditions, indicating a role for cytochrome localization to enabling survival in the electron donor and carbon-limited conditions. To determine which pathways enhanced growth using formate, Sequential Window Acquisition of all Theoretical Mass Spectra mass spectrometry (SWATH-MS) proteomics of formate adapted PilA-deficient mutants and acetate grown wild type was performed. PilA-deficient mutants had an overall decrease in tricarboxylic acid (TCA) cycle enzymes and significant upregulation of electron transport chain associated proteins including many c-type cytochromes and [NiFe]-hydrogenases. Whole genome sequencing of the mutants shows strong convergent evolution and emergence of genetic subpopulations during adaptation to growth on formate. The results described here suggest a role for membrane constrained c-type cytochromes to the enhancement of survival and growth in electron donor and carbon-limited conditions.

Keywords

Geobacter sulfurreducens SWATH-MS proteomics Whole genome sequencing Adaptive evolution Formate 

Notes

Acknowledgements

We would like to thank Dr. Derek Lovley for his generous gift of the G. sulfurreducens wild-type and ΔpilA mutant strains and Dr. Gemma Reguera for her generous gift of the G. sulfurreducens ΔpilB and ΔpilA (herein referred to as ΔpilA′) mutant strains.

Funding Information

This research has been partially financially supported by the Human Protection and Performance Program of the Defence Science Institute. The Applied and Environmental Microbiology Laboratory receives support from the Defence Science and Technology Group (DSTG), Office of Naval Research Global (Award no. N626909-13-1-N259), Asian Office of Aerospace Research and Development (AOARD; Award no. FA2386-14-1-4032), and the Australian Research Council (ARC; Award no. LP140100459).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2019_1316_MOESM1_ESM.pdf (191 kb)
Figure S1. Differences in G. sulfurreducens protein abundance from adapted G. sulfurreducens ΔpilA mutants in NB(formate/fumarate) vs. DL-1 wild-type grown in NB(acetate/fumarate). Volcano plots depicting significantly upregulated (pink dots) and downregulated (blue dots) G. sulfurreducens proteins in the ΔpilA s13 in NBFF versus DL-1 wild-type grown in NBAF. Green dots represent proteins that whose abundance was not significantly different between the cultures. Significance is defined as Log2FC values ≥ |1.0| and adjusted p-value ≤ 0.05 (PDF 191 kb)
248_2019_1316_MOESM2_ESM.pdf (48 kb)
Figure S2. Amino acid sequence of wild-type GSU0980 from G. sulfurreducens DL-1 wild-type grown in NBAF and single nucleotide insertion that causes a frameshift mutation in GSU0980 from G. sulfurreducens ΔpilA grown in NB(formate/fumarate). Alignment of sequencing reads against the reference G. sulfurreducens PCA genome was visualized on the IGV genome browser. Amino acid residues in red outline on genome browser inset and in red text of the peptide sequence represent those altered from the wild-type residues due to frameshift caused by the single nucleotide insertion event (PDF 48.4 kb)
248_2019_1316_MOESM3_ESM.xlsx (10 kb)
Table S1. Categories of cellular function and their associated KEGG pathways (XLSX 10 kb)
248_2019_1316_MOESM4_ESM.xlsx (35 kb)
Table S2. Summary of proteins and their log2fold difference in abundances (XLSX 34 kb)
248_2019_1316_MOESM5_ESM.xlsx (12 kb)
Table S3. Impacts of variants on predicted domains (XLSX 11 kb)

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Authors and Affiliations

  1. 1.Department of Physiology, Anatomy and MicrobiologyLa Trobe UniversityMelbourneAustralia
  2. 2.Bioinformatics and Cancer Genomics, Research DivisionPeter MacCallum Cancer CentreMelbourneAustralia
  3. 3.Advanced Water Management CentreThe University of QueenslandBrisbaneAustralia
  4. 4.Centre for Future LandscapesLa Trobe UniversityMelbourneAustralia

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