The impact of the cyanobacterial carbon-regulator protein SbtB and of the second messengers cAMP and c-di-AMP on CO2 -dependent gene expression

New Phytol. 2022 Jun;234(5):1801-1816. doi: 10.1111/nph.18094. Epub 2022 Apr 9.

Abstract

The amount of inorganic carbon (Ci ) fluctuates in aquatic environments. Cyanobacteria evolved a Ci -concentrating mechanism (CCM) that is regulated at different levels. The regulator SbtB binds to the second messengers cAMP or c-di-AMP and is involved in acclimation to low Ci (LC) in Synechocystis sp. PCC 6803. Here, we investigated the role of SbtB and of associated second messengers at different Ci conditions. The transcriptome of wild-type (WT) Synechocystis and the ΔsbtB mutant were compared with Δcya1, a mutant defective in cAMP production, and ΔdacA, a mutant defective in generating c-di-AMP. A defined subset of LC-regulated genes in the WT was already changed in ΔsbtB under high Ci (HC) conditions. This response of ΔsbtB correlated with a diminished induction of many CCM-associated genes after LC shift in this mutant. The Δcya1 mutant showed less deviation from WT, whereas ΔdacA induced CCM-associated genes under HC. Metabolome analysis also revealed differences between the strains, whereby ΔsbtB showed slower accumulation of 2-phosphoglycolate and ΔdacA differences among amino acids compared to WT. Collectively, these results indicate that SbtB regulates a subset of LC acclimation genes while c-di-AMP and especially cAMP appear to have a lesser impact on gene expression under different Ci availabilities.

Keywords: PII-like; c-di-AMP; inorganic carbon acclimation; photosynthesis; signaling; transcriptomics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Carbon Dioxide / metabolism
  • Carbon* / metabolism
  • Dinucleoside Phosphates
  • Gene Expression Regulation, Bacterial
  • Photosynthesis
  • Second Messenger Systems
  • Synechocystis* / genetics
  • Synechocystis* / metabolism
  • Transcriptome

Substances

  • Bacterial Proteins
  • Dinucleoside Phosphates
  • cyclic diadenosine phosphate
  • Carbon Dioxide
  • Carbon