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Research Article

The essential gene set of a photosynthetic organism

Benjamin E. Rubin, Kelly M. Wetmore, Morgan N. Price, Spencer Diamond, Ryan K. Shultzaberger, Laura C. Lowe, Genevieve Curtin, Adam P. Arkin, Adam Deutschbauer, and Susan S. Golden
PNAS December 1, 2015 112 (48) E6634-E6643; first published October 27, 2015; https://doi.org/10.1073/pnas.1519220112
Benjamin E. Rubin
aDivision of Biological Sciences, University of California, San Diego, La Jolla, CA 92093;
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Kelly M. Wetmore
bPhysical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
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Morgan N. Price
bPhysical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
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Spencer Diamond
aDivision of Biological Sciences, University of California, San Diego, La Jolla, CA 92093;
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Ryan K. Shultzaberger
cKavli Institute for Brain and Mind, University of California, San Diego, La Jolla, CA 92093;
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Laura C. Lowe
aDivision of Biological Sciences, University of California, San Diego, La Jolla, CA 92093;
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Genevieve Curtin
aDivision of Biological Sciences, University of California, San Diego, La Jolla, CA 92093;
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Adam P. Arkin
bPhysical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
dDepartment of Bioengineering, University of California, Berkeley, CA 94720
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Adam Deutschbauer
bPhysical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
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Susan S. Golden
aDivision of Biological Sciences, University of California, San Diego, La Jolla, CA 92093;
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  • For correspondence: sgolden@ucsd.edu
  1. Contributed by Susan S. Golden, September 29, 2015 (sent for review July 16, 2015; reviewed by Caroline S. Harwood and William B. Whitman)

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Significance

Cyanobacteria are model organisms for photosynthesis in the laboratory, are key producers of the chemical energy that drives life, and are being developed as biofuel and chemical producers for industry. Despite the importance of these organisms for environmental and biotechnological applications, only a small percentage of cyanobacterial genes and intergenic regions have been experimentally evaluated for their impact on the organisms’ survival. Here, we present experimental analysis of the complete set of genomic regions necessary for survival in a cyanobacterium achieved by screening for the fitness of hundreds of thousands of mutants. In addition to improving our fundamental understanding of Cyanobacteria, this research more broadly provides a snapshot of the essential genes and intergenic regions necessary to live the photosynthetic lifestyle.

Abstract

Synechococcus elongatus PCC 7942 is a model organism used for studying photosynthesis and the circadian clock, and it is being developed for the production of fuel, industrial chemicals, and pharmaceuticals. To identify a comprehensive set of genes and intergenic regions that impacts fitness in S. elongatus, we created a pooled library of ∼250,000 transposon mutants and used sequencing to identify the insertion locations. By analyzing the distribution and survival of these mutants, we identified 718 of the organism’s 2,723 genes as essential for survival under laboratory conditions. The validity of the essential gene set is supported by its tight overlap with well-conserved genes and its enrichment for core biological processes. The differences noted between our dataset and these predictors of essentiality, however, have led to surprising biological insights. One such finding is that genes in a large portion of the TCA cycle are dispensable, suggesting that S. elongatus does not require a cyclic TCA process. Furthermore, the density of the transposon mutant library enabled individual and global statements about the essentiality of noncoding RNAs, regulatory elements, and other intergenic regions. In this way, a group I intron located in tRNALeu, which has been used extensively for phylogenetic studies, was shown here to be essential for the survival of S. elongatus. Our survey of essentiality for every locus in the S. elongatus genome serves as a powerful resource for understanding the organism’s physiology and defines the essential gene set required for the growth of a photosynthetic organism.

  • RB-TnSeq
  • transposon mutagenesis
  • Tn-seq
  • cyanobacteria
  • photosynthesis

Footnotes

  • ↵1To whom correspondence should be addressed. Email: sgolden{at}ucsd.edu.
  • Author contributions: B.E.R., K.M.W., S.D., A.D., and S.S.G. designed research; B.E.R., K.M.W., M.N.P., R.K.S., L.C.L., and G.C. performed research; K.M.W., M.N.P., A.P.A., and A.D. contributed new reagents/analytic tools; B.E.R., M.N.P., S.D., R.K.S., and S.S.G. analyzed data; and B.E.R. and S.S.G. wrote the paper.

  • Reviewers: C.S.H., University of Washington; and W.B.W., The University of Georgia.

  • The authors declare no conflict of interest.

  • See Commentary on page 14747.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1519220112/-/DCSupplemental.

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Photosynthetic essential gene set
Benjamin E. Rubin, Kelly M. Wetmore, Morgan N. Price, Spencer Diamond, Ryan K. Shultzaberger, Laura C. Lowe, Genevieve Curtin, Adam P. Arkin, Adam Deutschbauer, Susan S. Golden
Proceedings of the National Academy of Sciences Dec 2015, 112 (48) E6634-E6643; DOI: 10.1073/pnas.1519220112

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Photosynthetic essential gene set
Benjamin E. Rubin, Kelly M. Wetmore, Morgan N. Price, Spencer Diamond, Ryan K. Shultzaberger, Laura C. Lowe, Genevieve Curtin, Adam P. Arkin, Adam Deutschbauer, Susan S. Golden
Proceedings of the National Academy of Sciences Dec 2015, 112 (48) E6634-E6643; DOI: 10.1073/pnas.1519220112
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