Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 106, Issue 15, Pages 6345-6350Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.0810547106
Keywords
NanoSIMS; stable isotope labeling; cyanophycin
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Funding
- U. S. Department of Education Office of Biological and Environmental Research Genomics Genomes to Life Research Program
- National Science Foundation Ocean Science Program [OCE 0452765, OCE 0753218]
- U. S. Department of Energy [DE-AC52-07NA27344]
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The marine cyanobacterium Trichodesmium is ubiquitous in tropical and subtropical seas and is an important contributor to global N and C cycling. We sought to characterize metabolic uptake patterns in individual Trichodesmium IMS-101 cells by quantitatively imaging C-13 and N-15 uptake with high-resolution secondary ion mass spectrometry (NanoSIMS). Trichodesmium fix both CO2 and N-2 concurrently during the day and are, thus, faced with a balancing act: the O-2 evolved during photosynthesis inhibits nitrogenase, the key enzyme in N-2 fixation. After performing correlated transmission electron microscopy (TEM) and NanoSIMS analysis on trichome thin-sections, we observed transient inclusion of N-15 and C-13 into discrete subcellular bodies identified as cyanophycin granules. We speculate that Trichodesmium uses these dynamic storage bodies to uncouple CO2 and N-2 fixation from overall growth dynamics. We also directly quantified both CO2 and N-2 fixation at the single cell level using NanoSIMS imaging of whole cells in multiple trichomes. Our results indicate maximal CO2 fixation rates in the morning, compared with maximal N-2 fixation rates in the afternoon, bolstering the argument that segregation of CO2 and N-2 fixation in Trichodesmium is regulated in part by temporal factors. Spatial separation of N-2 and CO2 fixation may also have a role in metabolic segregation in Trichodesmium. Our approach in combining stable isotope labeling with NanoSIMS and TEM imaging can be extended to other physiologically relevant elements and processes in other important microbial systems.
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