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Title: Metagenomic Analysis of the Indian Ocean Picocyanobacterial Community: Structure, Potential Function and Evolution

Abstract

Unicellular cyanobacteria are ubiquitous photoautotrophic microbes that contribute substantially to global primary production. Picocyanobacteria such as Synechococcus and Prochlorococcus depend on chlorophyll a-binding protein complexes to capture light energy. In addition, Synechococcus has accessory pigments organized into phycobilisomes, and Prochlorococcus contains chlorophyll b. Across a surface water transect spanning the sparsely studied tropical Indian Ocean, we examined Synechococcus and Prochlorococcus occurrence, taxonomy and habitat preference in an evolutionary context. Shotgun sequencing of size fractionated microbial communities from 0.1 μm to 20 μm and subsequent phylogenetic analysis indicated that cyanobacteria account for up to 15% of annotated reads, with the genera Prochlorococcus and Synechococcus comprising 90% of the cyanobacterial reads, even in the largest size fraction (3.0–20 mm). Phylogenetic analyses of cyanobacterial light-harvesting genes (chl-binding pcb/isiA, allophycocyanin ( apcAB), phycocyanin ( cpcAB) and phycoerythin ( cpeAB)) mostly identified picocyanobacteria clades comprised of overlapping sequences obtained from Indian Ocean, Atlantic and/or Pacific Oceans samples. Habitat reconstructions coupled with phylogenetic analysis of the Indian Ocean samples suggested that large Synechococcus-like ancestors in coastal waters expanded their ecological niche towards open oligotrophic waters in the Indian Ocean through lineage diversification and associated streamlining of genomes (e.g. loss of phycobilisomes and acquisition of Chl b);more » resulting in contemporary small celled Prochlorococcus. As a result, comparative metagenomic analysis with picocyanobacteria populations in other oceans suggests that this evolutionary scenario may be globally important.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [4];  [6];  [3];  [7]
  1. Pontificia Univ. Catolica de Chile, Santiago (Chile); Stockholm Univ., Solna (Sweden); Center for Climate Change and Resilience Research (CR)2, Santiago (Chile)
  2. Stockholm Univ., Solna (Sweden); Swedish Museum of Natural History, Stockholm (Sweden)
  3. Stockholm Univ., Solna (Sweden)
  4. J. Craig Venter Institute, San Diego, CA (United States)
  5. J. Craig Venter Institute, San Diego, CA (United States); Univ. of California San Diego, La Jolla, CA (United States)
  6. J. Craig Venter Institute, Rockville, MD (United States); Indiana Univ., Bloomington, IN (United States)
  7. CSIR-National Institute of Oceanography (India)
Publication Date:
Research Org.:
Stockholm Univ., Solna (Sweden)
Sponsoring Org.:
USDOE
OSTI Identifier:
1377077
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Indian Ocean; Synechococcus; Marine ecology; Oceans; Costal ecology; Metagenomics; Cyanobacteria; Phylogenetic analysis

Citation Formats

Diez, Beatriz, Nylander, Johan A. A., Ininbergs, Karolina, Dupont, Christopher L., Allen, Andrew E., Yooseph, Shibu, Rusch, Douglas B., Bergman, Birgitta, and Anil, Arga Chandrashekar. Metagenomic Analysis of the Indian Ocean Picocyanobacterial Community: Structure, Potential Function and Evolution. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0155757.
Diez, Beatriz, Nylander, Johan A. A., Ininbergs, Karolina, Dupont, Christopher L., Allen, Andrew E., Yooseph, Shibu, Rusch, Douglas B., Bergman, Birgitta, & Anil, Arga Chandrashekar. Metagenomic Analysis of the Indian Ocean Picocyanobacterial Community: Structure, Potential Function and Evolution. United States. doi:10.1371/journal.pone.0155757.
Diez, Beatriz, Nylander, Johan A. A., Ininbergs, Karolina, Dupont, Christopher L., Allen, Andrew E., Yooseph, Shibu, Rusch, Douglas B., Bergman, Birgitta, and Anil, Arga Chandrashekar. Thu . "Metagenomic Analysis of the Indian Ocean Picocyanobacterial Community: Structure, Potential Function and Evolution". United States. doi:10.1371/journal.pone.0155757. https://www.osti.gov/servlets/purl/1377077.
@article{osti_1377077,
title = {Metagenomic Analysis of the Indian Ocean Picocyanobacterial Community: Structure, Potential Function and Evolution},
author = {Diez, Beatriz and Nylander, Johan A. A. and Ininbergs, Karolina and Dupont, Christopher L. and Allen, Andrew E. and Yooseph, Shibu and Rusch, Douglas B. and Bergman, Birgitta and Anil, Arga Chandrashekar},
abstractNote = {Unicellular cyanobacteria are ubiquitous photoautotrophic microbes that contribute substantially to global primary production. Picocyanobacteria such as Synechococcus and Prochlorococcus depend on chlorophyll a-binding protein complexes to capture light energy. In addition, Synechococcus has accessory pigments organized into phycobilisomes, and Prochlorococcus contains chlorophyll b. Across a surface water transect spanning the sparsely studied tropical Indian Ocean, we examined Synechococcus and Prochlorococcus occurrence, taxonomy and habitat preference in an evolutionary context. Shotgun sequencing of size fractionated microbial communities from 0.1 μm to 20 μm and subsequent phylogenetic analysis indicated that cyanobacteria account for up to 15% of annotated reads, with the genera Prochlorococcus and Synechococcus comprising 90% of the cyanobacterial reads, even in the largest size fraction (3.0–20 mm). Phylogenetic analyses of cyanobacterial light-harvesting genes (chl-binding pcb/isiA, allophycocyanin (apcAB), phycocyanin (cpcAB) and phycoerythin (cpeAB)) mostly identified picocyanobacteria clades comprised of overlapping sequences obtained from Indian Ocean, Atlantic and/or Pacific Oceans samples. Habitat reconstructions coupled with phylogenetic analysis of the Indian Ocean samples suggested that large Synechococcus-like ancestors in coastal waters expanded their ecological niche towards open oligotrophic waters in the Indian Ocean through lineage diversification and associated streamlining of genomes (e.g. loss of phycobilisomes and acquisition of Chl b); resulting in contemporary small celled Prochlorococcus. As a result, comparative metagenomic analysis with picocyanobacteria populations in other oceans suggests that this evolutionary scenario may be globally important.},
doi = {10.1371/journal.pone.0155757},
journal = {PLoS ONE},
number = 5,
volume = 11,
place = {United States},
year = {Thu May 19 00:00:00 EDT 2016},
month = {Thu May 19 00:00:00 EDT 2016}
}

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