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Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria

  1. Laurence Garczareka,3
  1. aSorbonne Universités, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff, France;
  2. bDepartment of Marine Biology and Oceanography, Institute of Marine Sciences (ICM), Consejo Superior de Investigaciones Científicas (CSIC), Barcelona ES-08003, Spain;
  3. cDepartment of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, NSW 2109, Australia;
  4. dSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom;
  5. eCommissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Institut de Génomique, Genoscope, 91057 Evry, France;
  6. fStazione Zoologica Anton Dohrn, 80121 Naples, Italy

  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved May 6, 2016 (received for review January 5, 2016)

Significance

Metagenomics has become an accessible approach to study complex microbial communities thanks to the advent of high-throughput sequencing technologies. However, molecular ecology studies often face interpretation issues, notably due to the lack of reliable reference databases for assigning reads to the correct taxa and use of fixed cutoffs to delineate taxonomic groups. Here, we considerably refined the phylogeography of marine picocyanobacteria, responsible for about 25% of global marine productivity, by recruiting reads targeting a high-resolution marker from Tara Oceans metagenomes. By clustering lineages based on their distribution patterns, we showed that there is significant diversity at a finer resolution than the currently defined “ecotypes,” a diversity that is tightly controlled by environmental cues.

Abstract

Prochlorococcus and Synechococcus are the two most abundant and widespread phytoplankton in the global ocean. To better understand the factors controlling their biogeography, a reference database of the high-resolution taxonomic marker petB, encoding cytochrome b6, was used to recruit reads out of 109 metagenomes from the Tara Oceans expedition. An unsuspected novel genetic diversity was unveiled within both genera, even for the most abundant and well-characterized clades, and 136 divergent petB sequences were successfully assembled from metagenomic reads, significantly enriching the reference database. We then defined Ecologically Significant Taxonomic Units (ESTUs)—that is, organisms belonging to the same clade and occupying a common oceanic niche. Three major ESTU assemblages were identified along the cruise transect for Prochlorococcus and eight for Synechococcus. Although Prochlorococcus HLIIIA and HLIVA ESTUs codominated in iron-depleted areas of the Pacific Ocean, CRD1 and the yet-to-be cultured EnvB were the prevalent Synechococcus clades in this area, with three different CRD1 and EnvB ESTUs occupying distinct ecological niches with regard to iron availability and temperature. Sharp community shifts were also observed over short geographic distances—for example, around the Marquesas Islands or between southern Indian and Atlantic Oceans—pointing to a tight correlation between ESTU assemblages and specific physico-chemical parameters. Together, this study demonstrates that there is a previously overlooked, ecologically meaningful, fine-scale diversity within some currently defined picocyanobacterial ecotypes, bringing novel insights into the ecology, diversity, and biology of the two most abundant phototrophs on Earth.

Footnotes

  • ↵1G.K.F. and H.D. contributed equally to this work.

  • ↵2Present address: Food Safety, Environment, and Genetics, Matís Ltd., 113 Reykjavík, Iceland.

  • ↵3To whom correspondence should be addressed. Email: laurence.garczarek{at}sb-roscoff.fr.

  • Author contributions: G.K.F. and L.G. designed research; G.K.F., H.D., and M.R. performed research; M.O., F.D.P., P.W., D.J.S., and S.G.A. contributed new reagents/analytic tools; M.O., F.D.P., and D.J.S. provided petB reference sequences; P.W. provided sequencing of the metagenomic dataset; G.K.F., H.D., F.M.C.-C., D.I., and L.G. analyzed data; and G.K.F., H.D., F.P., and L.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KU377785-990, KU670814-6, KU705397-460, and KU937818-30).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1524865113/-/DCSupplemental.

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