Low temporal dynamics of mycosporine-like amino acids in benthic cyanobacteria from an alpine lake.

Nadine Werner, Maria Orfanoudaki, Anja Hartmann, Markus Ganzera, Ruben Sommaruga
Author Information
  1. Nadine Werner: Department of Ecology University of Innsbruck Innsbruck Austria.
  2. Maria Orfanoudaki: Institute of Pharmacy Pharmacognosy University of Innsbruck Innsbruck Austria.
  3. Anja Hartmann: Institute of Pharmacy Pharmacognosy University of Innsbruck Innsbruck Austria.
  4. Markus Ganzera: Institute of Pharmacy Pharmacognosy University of Innsbruck Innsbruck Austria.
  5. Ruben Sommaruga: Department of Ecology University of Innsbruck Innsbruck Austria. ORCID

Abstract

Cyanobacteria are one of the oldest organisms on Earth and they originated at a time when damaging ultraviolet (UV) C radiation still reached the surface. Their long evolution led to several adaptations to avoid deleterious effects caused by exposure to solar UV radiation. Synthesis of sunscreen substances, such as mycosporine-like amino acids (MAAs), allows them to photosynthesise with reduced risk of cell damage. The interplay of solar UV radiation and MAAs is well documented for cyanobacteria in the plankton realm, but little is known for those in the benthic realm, particularly of clear alpine lakes.Here, we assessed the temporal dynamics of MAAs in the benthic algal community of one clear alpine lake dominated by cyanobacteria during the ice-free season and along a depth gradient using state-of-the-art analytical methods (high-performance liquid chromatography, nuclear magnetic resonance, liquid chromatography-mass spectrometry). We differentiated between the epilithic cyanobacterial community and the overlying loosely attached filamentous cyanobacteria, as we expected they will have an important shielding/shading effect on the former. We hypothesised that in contrast to the case of phytoplankton, benthic cyanobacteria will show less pronounced temporal changes in MAAs concentration in response to changes in solar UV exposure.Three UV-absorbing substances were present in both types of communities, whereby all were unknown. The chemical structure of the dominant unknown substance (maximum absorption at 334 nm) resulted in the identification of a novel MAA that we named aplysiapalythine-D for its similarity to the previously described aplysiapalythine-C.Chlorophyll--specific MAA concentrations for epilithic and filamentous cyanobacteria showed a significant decrease with depth, although only traces were found in the former community. The temporal dynamics in MAA concentrations of filamentous cyanobacteria showed no significant variations during the ice-free season.Our result on the low temporal MAA dynamics agrees with the reduced growth rates of benthic cyanobacteria reported for cold ecosystems. The permanent presence of this community, which is adapted to the high UV levels characteristic of clear alpine lakes, probably represents the most important primary producers of these ecosystems.

Keywords

References

  1. J Photochem Photobiol B. 2015 Aug;149:149-55 [PMID: 26065817]
  2. J Photochem Photobiol B. 2014 Dec;141:154-69 [PMID: 25463663]
  3. J Plankton Res. 2014 Mar;36(2):557-566 [PMID: 24616551]
  4. Nat Rev Microbiol. 2011 Oct 03;9(11):791-802 [PMID: 21963801]
  5. J Phycol. 2019 Apr;55(2):393-403 [PMID: 30565696]
  6. J Photochem Photobiol B. 2011 Oct 5;105(1):81-9 [PMID: 21813286]
  7. Mar Drugs. 2020 Jan 24;18(2): [PMID: 31991623]
  8. Nature. 2008 Oct 23;455(7216):1051-2 [PMID: 18948942]
  9. Appl Environ Microbiol. 1993 Jan;59(1):163-9 [PMID: 16348839]
  10. J Photochem Photobiol B. 2001 Sep 1;62(1-2):35-42 [PMID: 11693365]
  11. Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11494-9 [PMID: 21709250]
  12. Biol Rev Camb Philos Soc. 1999 Aug;74(3):311-45 [PMID: 10466253]
  13. Antioxidants (Basel). 2015 Sep 07;4(3):603-46 [PMID: 26783847]
  14. Biochimie. 2018 Nov;154:35-44 [PMID: 30071261]
  15. FEMS Microbiol Ecol. 2005 Jun 1;53(1):73-87 [PMID: 16329931]
  16. Freshw Biol. 2021 Jan;66(1):169-176 [PMID: 33510548]
  17. Rapid Commun Mass Spectrom. 2020 Sep;34 Suppl 3:e8634 [PMID: 31677357]
  18. Appl Environ Microbiol. 2016 Sep 16;82(19):5951-9 [PMID: 27474710]
  19. Appl Environ Microbiol. 1995 Dec;61(12):4215-22 [PMID: 16535178]
  20. Environ Technol. 2012 Jan-Feb;33(1-3):153-7 [PMID: 22519098]
  21. J Photochem Photobiol B. 2019 Dec;201:111684 [PMID: 31733505]
  22. Limnol Oceanogr. 2006 May;51(3):1530-1541 [PMID: 21258624]

Grants

  1. P 29671/Austrian Science Fund FWF

Word Cloud

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