Abstract
Experimentation at sea provides insight into which traits of ocean microbes are linked to performance in situ. Here we show distinct patterns in thermal tolerance of microbial phototrophs from adjacent water masses sampled in the south-west Pacific Ocean, determined using a fluorescent marker for reactive oxygen species (ROS). ROS content of pico-eukaryotes was assessed after 1, 5 and 25 h of incubation along a temperature gradient (15.6–32.1 °C). Pico-eukaryotes from the East Australian Current (EAC) had relatively constant ROS and showed greatest mortality after 25 h at 7 °C below ambient, whereas those from the Tasman Sea had elevated ROS in both warm and cool temperature extremes and greatest mortality at temperatures 6–10 °C above ambient, interpreted as the outcome of thermal stress. Tracking of water masses within an oceanographic circulation model showed populations had distinct thermal histories, with EAC pico-eukaryotes experiencing higher average temperatures for at least 1 week prior to sampling. While acclimatization and community assembly could both influence biological responses, this study clearly demonstrates that phenotypic divergence occurs along planktonic drift trajectories.
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Barton AD, Irwin AJ, Finkel ZV, Stock CA. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc Nat Acad Sci. 2016;113:2964–9.
Dutkiewicz S, Scott J, Follows MJ. Winners and losers: ecological and biogeochemical changes in a warming ocean. Glob Biogeochem Cycles. 2013;27:463–77.
Fuhrman JA, Cram JA, Needham DM. Marine microbial cymmunity dynamics and their ecological interpretation. Nat Microbiol. 2015;13:133–46.
Listmann L, LeRoch M, Schluter L, Thomas M, Reusch TBH. Swift thermal reaction norm evoluation in a key marine phytoplankton species. Evol Appl. 2016;9:1156–64.
Schulte PM, Healy TM, Fangue NA. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol. 2011;51:691–702.
Doblin MA, van Sebille E. Drift in ocean currents impacts intergenerational microbial exposure to temperature. Proc Nat Acad Sci. 2016;113:5700–5.
Wu L, Cai W, Zhang W, Nakamura H, Timmermann A, Joyce T, et al. Enhanced warming over the global subtropical western boundary currents. Nat Clim Change. 2012;2:161–6.
Ruderman D. The emergence of dynamic phenotyping. Cell Biol Toxicol. 2017;33:507–9.
Cruz JA, Savage LJ, Zegarac R, Hall CC, Satoh-Cruz M, Davis GA, et al. Dynamic environmental photosynthetic imaging reveals emergent phenotypes. Cell Syst. 2016;2:365–77.
Middlebrook R, Hoegh-Guldberg O, Leggat W (2008). The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biology 211:1050–56.
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidativestress, and signal transduction. Ann Rev Plant Biol. 2004;55:373–99.
Gill SS, Tuyeja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48:909–30.
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, et al. ROS signaling: the new wave? Trends Plant Sci. 2011;16:300–9.
Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006;141:391–6.
Perez-Perez ME, Lemaire SD, Crespo JL. Reactive oxygen species and autophagy in plants and algae. Plant Physiol. 2012;160:156–64.
Decelle J, Romac S, Stern RF, Bendif EM, Zingone A, Audic S, et al. PhytoREF: a reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Mol Ecol Res. 2015;15:1435–45.
Vannier T, Leconte J, Seeleuthner Y, Mondy S, Pelletier E, Aury JM. et al. Survey of the green picoalga Bathycoccus genomes in the global ocean. Nature Sci Rep. 2016;6:37900
Pospíšil P. Production of reactive oxygen species by photosystem II. Biochim Et Biophys Acta. 2009;1787:1151–60.
Feder ME, Hoffman GE. Heat shock proteins, molecular chaperones, and the stress response. Ann Rev Physiol. 1999;61:243–82.
Henkel SK, Hoffman GE. Differing patterns of hsp70 gene expression in invasive and native kelp species: evidence for acclimation-induced variation. J Appl Phycol. 2008;20:915–24.
Acknowledgements
The authors would like to thank the Marine National Facility for ship-time and technical support on the RV Investigator, as well as the captain, crew, and chief scientist, Prof Iain Suthers, for facilitating our sample collection during voyage IN2015_V03. This research was supported by an Australian Research Council Discovery Project (DP14010134) and Large Infrastructure and Equipment Fund (LE130100019) to MD. Molecular analyses were funded by an ARC Discovery Grant (DP140101045), awarded to Prof Justin Seymour; we thank him and Dr Nahshon Siboni for their support. CTK was supported by NSF grant OCE-1638958, MEL, KGB, JSC, CMR, LL and MA were supported by Australian Government Training Program Scholarships and OFL was funded by a University of Technology Sydney Chancellor’s Postdoctoral Fellowship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
McInnes, A.S., Laczka, O.F., Baker, K.G. et al. Live cell analysis at sea reveals divergent thermal performance between photosynthetic ocean microbial eukaryote populations. ISME J 13, 1374–1378 (2019). https://doi.org/10.1038/s41396-019-0355-6
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-019-0355-6