TY - JOUR
T1 - Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans
AU - Liu, Hui
AU - Probert, Ian
AU - Uitz, Julia
AU - Claustre, Hervé
AU - Aris-Brosou, Stéphane
AU - Frada, Miguel
AU - Not, Fabrice
AU - De Vargas, Colomban
PY - 2009/8/4
Y1 - 2009/8/4
N2 - 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.
AB - 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.
KW - Eukaryotic biodiversity
KW - Haptophyta
KW - Photosynthesis
KW - Protistan biodiversity
UR - http://www.scopus.com/inward/record.url?scp=69149100641&partnerID=8YFLogxK
U2 - 10.1073/pnas.0905841106
DO - 10.1073/pnas.0905841106
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C2 - 19622724
AN - SCOPUS:69149100641
SN - 0027-8424
VL - 106
SP - 12803
EP - 12808
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 31
ER -