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Daily bursts of biogenic cyanogen bromide (BrCN) control biofilm formation around a marine benthic diatom

Bart Vanelslander UGent, Carsten Paul, Jan Grueneberg, Emily K Prince, Jeroen Gillard UGent, Koen Sabbe UGent, Georg Pohnert and Wim Vyverman UGent (2012) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 109(7). p.2412-2417
abstract
The spatial organization of biofilms is strongly regulated by chemical cues released by settling organisms. However, the exact nature of these interactions and the repertoire of chemical cues and signals that micro-organisms produce and exude in response to the presence of competitors remain largely unexplored. Biofilms dominated by microalgae often show remarkable, yet unexplained fine-scale patchy variation in species composition. Because this occurs even in absence of abiotic heterogeneity, antagonistic interactions might play a key role. Here we show that a marine benthic diatom produces chemical cues that cause chloroplast bleaching, a reduced photosynthetic efficiency, growth inhibition and massive cell death in naturally co-occurring competing microalgae. Using headspace solid phase microextraction (HS-SPME)-GC-MS, we demonstrate that this diatom exudes a diverse mixture of volatile iodinated and brominated metabolites including the natural product cyanogen bromide (BrCN), which exhibits pronounced allelopathic activity. Toxin production is light-dependent with a short BrCN burst after sunrise. BrCN acts as a short-term signal, leading to daily "cleaning" events around the algae. We show that allelopathic effects are H2O2 dependent and link BrCN production to haloperoxidase activity. This strategy is a highly effective means of biofilm control and may provide an explanation for the poorly understood role of volatile halocarbons from marine algae, which contribute significantly to the atmospheric halocarbon budget.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
chemical ecology, signal molecule, allelopathy, marine ecology, ICE ALGAE, BROMOPEROXIDASE, IODOPEROXIDASE, ALLELOPATHY, PROTECTION, MECHANISM, CULTURES, RELEASE, ENZYMES, BIOLOGY
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. USA
volume
109
issue
7
pages
2412 - 2417
Web of Science type
Article
Web of Science id
000300489200053
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
9.737 (2012)
JCR rank
4/56 (2012)
JCR quartile
1 (2012)
ISSN
0027-8424
DOI
10.1073/pnas.1108062109
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1987789
handle
http://hdl.handle.net/1854/LU-1987789
date created
2012-01-16 19:09:43
date last changed
2012-05-31 13:49:18
@article{1987789,
  abstract     = {The spatial organization of biofilms is strongly regulated by chemical cues released by settling organisms. However, the exact nature of these interactions and the repertoire of chemical cues and signals that micro-organisms produce and exude in response to the presence of competitors remain largely unexplored. Biofilms dominated by microalgae often show remarkable, yet unexplained fine-scale patchy variation in species composition. Because this occurs even in absence of abiotic heterogeneity, antagonistic interactions might play a key role. Here we show that a marine benthic diatom produces chemical cues that cause chloroplast bleaching, a reduced photosynthetic efficiency, growth inhibition and massive cell death in naturally co-occurring competing microalgae. Using headspace solid phase microextraction (HS-SPME)-GC-MS, we demonstrate that this diatom exudes a diverse mixture of volatile iodinated and brominated metabolites including the natural product cyanogen bromide (BrCN), which exhibits pronounced allelopathic activity. Toxin production is light-dependent with a short BrCN burst after sunrise. BrCN acts as a short-term signal, leading to daily {\textacutedbl}cleaning{\textacutedbl} events around the algae. We show that allelopathic effects are H2O2 dependent and link BrCN production to haloperoxidase activity. This strategy is a highly effective means of biofilm control and may provide an explanation for the poorly understood role of volatile halocarbons from marine algae, which contribute significantly to the atmospheric halocarbon budget.},
  author       = {Vanelslander, Bart and Paul, Carsten and Grueneberg, Jan and Prince, Emily K and Gillard, Jeroen and Sabbe, Koen and Pohnert, Georg and Vyverman, Wim},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {chemical ecology,signal molecule,allelopathy,marine ecology,ICE ALGAE,BROMOPEROXIDASE,IODOPEROXIDASE,ALLELOPATHY,PROTECTION,MECHANISM,CULTURES,RELEASE,ENZYMES,BIOLOGY},
  language     = {eng},
  number       = {7},
  pages        = {2412--2417},
  title        = {Daily bursts of biogenic cyanogen bromide (BrCN) control biofilm formation around a marine benthic diatom},
  url          = {http://dx.doi.org/10.1073/pnas.1108062109},
  volume       = {109},
  year         = {2012},
}

Chicago
Vanelslander, Bart, Carsten Paul, Jan Grueneberg, Emily K Prince, Jeroen Gillard, Koen Sabbe, Georg Pohnert, and Wim Vyverman. 2012. “Daily Bursts of Biogenic Cyanogen Bromide (BrCN) Control Biofilm Formation Around a Marine Benthic Diatom.” Proceedings of the National Academy of Sciences of the United States of America 109 (7): 2412–2417.
APA
Vanelslander, B., Paul, C., Grueneberg, J., Prince, E. K., Gillard, J., Sabbe, K., Pohnert, G., et al. (2012). Daily bursts of biogenic cyanogen bromide (BrCN) control biofilm formation around a marine benthic diatom. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 109(7), 2412–2417.
Vancouver
1.
Vanelslander B, Paul C, Grueneberg J, Prince EK, Gillard J, Sabbe K, et al. Daily bursts of biogenic cyanogen bromide (BrCN) control biofilm formation around a marine benthic diatom. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2012;109(7):2412–7.
MLA
Vanelslander, Bart, Carsten Paul, Jan Grueneberg, et al. “Daily Bursts of Biogenic Cyanogen Bromide (BrCN) Control Biofilm Formation Around a Marine Benthic Diatom.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 109.7 (2012): 2412–2417. Print.