Peculiar citric acid cycle of hydrothermal vent chemolithoautotroph Hydrogenovibrio crunogenus, and insights into carbon metabolism by obligate autotrophs

Ishtiaque Quasem, Alexandra N. Achille, Brittany A. Caddick, Travis A. Carter, Camille Daniels, Jennifer A. Delaney, Vedad Delic, Kimberly A. Denton, Martina C. Duran, Marianne K. Fatica, Christopher M. Ference, Julie P. Galkiewicz, Ana M. Garcia, Jacqueline D. Hendrick, Steven A. Horton, Mey S. Kun, Phoebe W. Koch, Tien Min Lee, Christie R. McCabe, Sean McHaleLauren D. McDaniel, Damian M. Menning, Kristy J. Menning, Hamed Mirzaei-Souderjani, Salina Mostajabian, David A. Nicholson, Courtney K. Nugent, Nicholas P. Osman, Desiree I. Pappas, Andrea M. Rocha, Karyna Rosario, Haydn Rubelmann, Julie A. Schwartz, Kent W. Seeley, Christopher M. Staley, Elizabeth M. Wallace, Terianne M. Wong, Brian L. Zielinski, Thomas E. Hanson, Kathleen M. Scott

Research output: Contribution to journalLetterpeer-review

7 Scopus citations

Abstract

The genome sequence of the obligate chemolithoautotroph Hydrogenovibrio crunogenus paradoxically predicts a complete oxidative citric acid cycle (CAC). This prediction was tested by multiple approaches including whole cell carbon assimilation to verify obligate autotrophy, phylogenetic analysis of CAC enzyme sequences and enzyme assays. Hydrogenovibrio crunogenus did not assimilate any of the organic compounds provided (acetate, succinate, glucose, yeast extract, tryptone). Enzyme activities confirmed that its CAC is mostly uncoupled from the NADH pool. 2-Oxoglutarate:ferredoxin oxidoreductase activity is absent, though pyruvate:ferredoxin oxidoreductase is present, indicating that sequence-based predictions of substrate for this oxidoreductase were incorrect, and that H. crunogenus may have an incomplete CAC. Though the H. crunogenus CAC genes encode uncommon enzymes, the taxonomic distribution of their top matches suggests that they were not horizontally acquired. Comparison of H. crunogenus CAC genes to those present in other 'Proteobacteria' reveals that H. crunogenus and other obligate autotrophs lack the functional redundancy for the steps of the CAC typical for facultative autotrophs and heterotrophs, providing another possible mechanism for obligate autotrophy.

Original languageEnglish (US)
Article numberfnx148
JournalFEMS Microbiology Letters
Volume364
Issue number14
DOIs
StatePublished - Jul 1 2017
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported by the United States Department of Agriculture [Higher Education Challenge Grant number MOE-2008-02036] and the National Science Foundation [grant numbers NSF-MCB-0643713, NSF-IOS-1257532] to KMS.

Publisher Copyright:
© FEMS 2017.

Keywords

  • Central carbon metabolism
  • Citric acid cycle
  • Hydrothermal vent
  • Obligate autotroph

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