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Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer?

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Abstract

Sea ice is permeated by small brine channels, which are characterised by sub-zero temperatures and varying salinities. Despite sometimes extreme conditions a diverse fauna and flora thrives within the brine channels. The dominant calanoid copepods of Antarctic sea ice are Stephos longipes and Paralabidocera antarctica. Here, I report for the first time thermal hysteresis (TH) in the haemolymph of a crustacean, S. longipes, whereas P. antarctica has no such activity. TH, the non-colligative prevention of ice growth, seems to enable S. longipes to exploit all available microhabitats within sea ice, especially the surface layer, in which strong temperature fluctuations can occur. In contrast, P. antarctica only thrives within the lowermost centimetres of sea ice, where temperature fluctuations are moderate. S. longipes possesses two isoforms of a protein with TH activity. A high homology to a group of (putative) antifreeze proteins from diatoms, bacteria and a snow mold and, in contrast, no homologs in any metazoan lineage suggest that this protein was obtained through horizontal gene transfer (HGT). Further analysis of available sequence data from sea-ice organisms indicates that these antifreeze proteins were probably transferred horizontally several times. Temperature and salinity fluctuations within the brine channel system are proposed to provide “natural transformation” conditions enabling HGT and thus making this habitat a potential “hot spot” for HGT.

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Abbreviations

Aa:

Amino acid

AFP:

Antifreeze protein

AF(G)P:

Antifreeze(glyco)protein

eEF-1α:

Eukaryotic elongation factor 1 alpha

FSW:

Filtered seawater

HGT:

Horizontal gene transfer

HSP70:

Heat shock protein 70

RI:

Recrystallization inhibition

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SSH:

Suppression subtractive hybridization

TH:

Thermal hysteresis

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Acknowledgments

Thanks are first of all due to I. Werner for her support during all phases of this study. I am grateful to captains, crews and colleagues (especially S. Schnack-Schiel, H. Schünemann and M. Kramer) for their help during the expeditions with R/V Polarstern. I furthermore thank H.-O. Pörtner for the opportunity to work in his labs and especially M. Lucassen for providing excellent facilities and tips for molecular biological work. U. John is thanked for help with sequencing parts of the cDNA library, G. Hemmrich for help with clustering the ESTs, T. C. G. Bosch for providing the vector and bacteria for the recombinant expression experiment and G. Dieckmann and C. Uhlig for diatom cultures and cDNA. I would furthermore like to thank I. Werner, M. Kramer, S. Siebert and M. Lucassen for critically reading the manuscript and three anonymous reviewers for excellent comments.

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  1. Rainer Kiko

    Present address: Leibniz Institute of Marine Sciences, IFM-GEOMAR, Hohenbergstr. 2, 24105, Kiel, Germany

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  1. Institute for Polar Ecology, Wischhofstr. 1-3, Bldg. 12, 24148, Kiel, Germany

    Rainer Kiko

  2. Alfred-Wegener-Institute for Polar and Marine Research, Am Handelshafen 12, 27570, Bremerhaven, Germany

    Rainer Kiko

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Kiko, R. Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer?. Polar Biol 33, 543–556 (2010). https://doi.org/10.1007/s00300-009-0732-0

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