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Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans

  1. Hui Liua,b,
  2. Ian Proberta,
  3. Julia Uitzc,
  4. Hervé Claustred,
  5. Stéphane Aris-Brosoue,
  6. Miguel Fradab,
  7. Fabrice Nota and
  8. Colomban de Vargasa,b,1
  1. aCentre National de la Recherche Scientifique, Unité Mixte de Recherche 7144 and Université Pierre et Marie Curie Paris 06, Equipe Evolution du Plancton et Paléo-Océans, Station Biologique de Roscoff, 29682, France;
  2. bInstitute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901;
  3. cMarine Physical Laboratory, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA 92093-0238;
  4. dCentre National de la Recherche Scientifique, Unité Mixte de Recherche 7093 and Université Pierre et Marie Curie Paris 06, Laboratoire d'Océanographie de Villefranche/Mer, 06234, France; and
  5. eDepartment of Biology and Department of Mathematics and Statistics, University of Ottawa, Ottawa, ON, Canada K1N 6N5

  1. Communicated by W. A. Berggren, Woods Hole Oceanographic Institution, Woods Hole, MA, June 2, 2009 (received for review December 18, 2008)

Abstract

The current paradigm holds that cyanobacteria, which evolved oxygenic photosynthesis more than 2 billion years ago, are still the major light harvesters driving primary productivity in open oceans. Here we show that tiny unicellular eukaryotes belonging to the photosynthetic lineage of the Haptophyta are dramatically diverse and ecologically dominant in the planktonic photic realm. The use of Haptophyta-specific primers and PCR conditions adapted for GC-rich genomes circumvented biases inherent in classical genetic approaches to exploring environmental eukaryotic biodiversity and led to the discovery of hundreds of unique haptophyte taxa in 5 clone libraries from subpolar and subtropical oceanic waters. Phylogenetic analyses suggest that this diversity emerged in Paleozoic oceans, thrived and diversified in the permanently oxygenated Mesozoic Panthalassa, and currently comprises thousands of ribotypic species, belonging primarily to low-abundance and ancient lineages of the “rare biosphere.” This extreme biodiversity coincides with the pervasive presence in the photic zone of the world ocean of 19′-hexanoyloxyfucoxanthin (19-Hex), an accessory photosynthetic pigment found exclusively in chloroplasts of haptophyte origin. Our new estimates of depth-integrated relative abundance of 19-Hex indicate that haptophytes dominate the chlorophyll a-normalized phytoplankton standing stock in modern oceans. Their ecologic and evolutionary success, arguably based on mixotrophy, may have significantly impacted the oceanic carbon pump. These results add to the growing evidence that the evolution of complex microbial eukaryotic cells is a critical force in the functioning of the biosphere.

Footnotes

  • 1To whom correspondence should be addressed. E-mail: vargas{at}sb-roscoff.fr

  • Author contributions: C.d.V. designed research; H.L., I.P., J.U., H.C., M.F., and F.N. performed research; H.L., J.U., H.C., S.A.-B., F.N., and C.d.V. analyzed data; and I.P. and C.d.V. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0905841106/DCSupplemental.

  • ↵* Note that chloroplast genomes are typically not GC biased, meaning they are amenable to standard PCR protocols and may provide a more accurate view of the real phytoplanktonic diversity.

  • ↵† Complex mixotrophic regimes may also explain why none of the open ocean haptophytes are currently available in culture collections.

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