Biodiversity patterns of plankton assemblages at the extremes of the Red Sea.

The diversity of microbial plankton has received limited attention in the main basin of the Red Sea. This study investigates changes in the community composition and structure of prokaryotes and eukaryotes at the extremes of the Red Sea along cross-shelf gradients and between the surface and deep chlorophyll maximum. Using molecular methods to target both the 16S and 18S rRNA genes, it was observed that the dominant prokaryotic classes were Acidimicrobiia, Alphaproteobacteria and Cyanobacteria, regardless of the region and depth. The eukaryotes Syndiniophyceae and Dinophyceae between them dominated in the north, with Bacillariophyceae and Mamiellophyceae more prominent in the southern region. Significant differences were observed for prokaryotes and eukaryotes for region, depth and distance from shore. Similarly, it was noticed that communities became less similar with increasing distance from the shore. Canonical correspondence analysis at the class level showed that Mamiellophyceae and Bacillariophyceae correlated with increased nutrients and chlorophyll a found in the southern region, which is influenced by the input of Gulf of Aden Intermediate Water.

[1]  U. Sommer,et al.  Seasonal dynamics of phytoplankton in the Gulf of Aqaba, Red Sea , 2007, Hydrobiologia.

[2]  Christian Winter,et al.  Horizontal and vertical complexity of attached and free‐living bacteria of the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints , 2001 .

[3]  C. Duarte,et al.  Biomass distribution in marine planktonic communities , 1997 .

[4]  M. Behrenfeld.  Biology: Uncertain future for ocean algae , 2011 .

[5]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[6]  B. Jones,et al.  Molecular-based approaches to characterize coastal microbial community and their potential relation to the trophic state of Red Sea , 2015, Scientific Reports.

[7]  R. Franklin,et al.  Bacterial assemblages of the eastern Atlantic Ocean reveal both vertical and latitudinal biogeographic signatures , 2012 .

[8]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[9]  C. Lovejoy,et al.  Oceanographic structure drives the assembly processes of microbial eukaryotic communities , 2014, The ISME Journal.

[10]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[11]  D. Vaulot,et al.  Effects of inorganic and organic nutrient addition on a coastal microbial community (Isefjord, Denmark) , 2002 .

[12]  L. Levin,et al.  Microbial abundance and diversity patterns associated with sediments and carbonates from the methane seep environments of Hydrate Ridge, OR , 2014, Front. Mar. Sci..

[13]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[14]  Amy S. Bower,et al.  The transport of nutrient-rich Indian Ocean water through the Red Sea and into coastal reef systems , 2014 .

[15]  L. Zinger,et al.  Two decades of describing the unseen majority of aquatic microbial diversity , 2012, Molecular ecology.

[16]  H. Ducklow,et al.  Marine bacterial, archaeal and eukaryotic diversity and community structure on the continental shelf of the western Antarctic Peninsula , 2014 .

[17]  C. Maillard,et al.  and exchanges with the Indian Ocean In summer , 1986 .

[18]  Raymond N. Gorley,et al.  PERMANOVA+ for PRIMER. Guide to software and statistical methods , 2008 .

[19]  Adam Godzik,et al.  Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences , 2006, Bioinform..

[20]  E. Carmack,et al.  Smallest Algae Thrive As the Arctic Ocean Freshens , 2009, Science.

[21]  L. Riemann,et al.  Global patterns of diversity and community structure in marine bacterioplankton , 2006, Molecular ecology.

[22]  A. Poisson,et al.  Some aspects of biogeochemical cycles in the Red Sea with special reference to new observations made in summer 1982 , 1984 .

[23]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[24]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[25]  U. Sommer.  The scarcity of medium sized phytoplankton in the northern Red Sea explained by strong bottom -up and weak top-down control , 2000 .

[26]  Ibrahim Hoteit,et al.  Phytoplankton phenology indices in coral reef ecosystems: Application to ocean-color observations in the Red Sea , 2015 .

[27]  M. Magnani,et al.  Analysis of rRNA gene content in the Mediterranean dinoflagellate Alexandrium catenella and Alexandrium taylori: implications for the quantitative real-time PCR-based monitoring methods , 2010, Journal of Applied Phycology.

[28]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[29]  William E. Johns,et al.  Observations of the summer Red Sea circulation , 2007 .

[30]  P. Bork,et al.  Eukaryotic plankton diversity in the sunlit ocean , 2015, Science.

[31]  M. Nassar,et al.  Seasonal fluctuations of phytoplankton community and physico-chemical parameters of the north western part of the Red Sea, Egypt , 2014 .

[32]  H. Touliabah,et al.  Phytoplankton Composition at Jeddah Coast-Red Sea, Saudi Arabia in Relation to some Ecological Factors , 2010 .

[33]  U. Sommer,et al.  Ecohydrographic constraints on biodiversity and distribution of phytoplankton and zooplankton in coral reefs of the Red Sea, Saudi Arabia , 2015 .

[34]  D. Vaulot,et al.  Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. , 2007, Environmental microbiology.

[35]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[36]  X. Irigoien,et al.  Zooplankton diversity across three Red Sea reefs using pyrosequencing , 2014, Front. Mar. Sci..

[37]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[38]  Stéphane Audic,et al.  The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy , 2012, Nucleic Acids Res..

[39]  F. Azam,et al.  The Microbial Loop , 2007 .

[40]  André Antunes,et al.  Biogeography of pelagic bacterioplankton across an antagonistic temperature–salinity gradient in the Red Sea , 2012, Molecular ecology.

[41]  Osvaldo Ulloa,et al.  Structure and seasonal dynamics of the eukaryotic picophytoplankton community in a wind‐driven coastal upwelling ecosystem , 2011 .

[42]  Laure Guillou,et al.  Wide genetic diversity of picoplanktonic green algae (Chloroplastida) in the Mediterranean Sea uncovered by a phylum-biased PCR approach. , 2008, Environmental microbiology.

[43]  U. Stingl,et al.  Diversity of picoeukaryotes at an oligotrophic site off the Northeastern Red Sea Coast , 2013, Aquatic biosystems.

[44]  L. Amaral-Zettler,et al.  Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities , 2009, BMC Biology.

[45]  Ibrahim Hoteit,et al.  Remote Sensing the Phytoplankton Seasonal Succession of the Red Sea , 2013, PloS one.

[46]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[47]  C. Pedrós-Alió,et al.  Spatial patterns of bacterial richness and evenness in the NW Mediterranean Sea explored by pyrosequencing of the 16S rRNA , 2010 .

[48]  T. F. Hansen,et al.  Grazing during early spring in the Gulf of Aqaba and the northern Red Sea , 2002 .

[49]  T. Stoeck,et al.  Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water , 2010, Molecular ecology.

[50]  Ibrahim Hoteit,et al.  Seasonal overturning circulation in the Red Sea: 1. Model validation and summer circulation , 2014 .

[51]  I. Hoteit,et al.  Thermocline Regulated Seasonal Evolution of Surface Chlorophyll in the Gulf of Aden , 2015, PloS one.

[52]  J. Roff,et al.  Phytoplankton ecology and production in the Red Sea off Jiddah, Saudi Arabia , 1986 .

[53]  D. Vaulot,et al.  Photosynthetic picoeukaryote community structure in the South East Pacific Ocean encompassing the most oligotrophic waters on Earth. , 2009, Environmental microbiology.

[54]  C. Duarte,et al.  Phytoplankton chlorophyll a distribution and water column stability in the central Atlantic Ocean , 1999 .

[55]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[56]  D. Vaulot,et al.  Protistan assemblages across the Indian Ocean, with a specific emphasis on the picoeukaryotes , 2008 .

[57]  Ajai,et al.  Comparative Analysis of Sea Surface Temperature Pattern in the Eastern and Western Gulfs of Arabian Sea and the Red Sea in Recent Past Using Satellite Data , 2013 .

[58]  Curtis A Suttle,et al.  Sequence Analysis of Marine Virus Communities Reveals that Groups of Related Algal Viruses Are Widely Distributed in Nature , 2002, Applied and Environmental Microbiology.

[59]  Andrew J. Alverson,et al.  INTRAGENOMIC NUCLEOTIDE POLYMORPHISM AMONG SMALL SUBUNIT (18S) RDNA PARALOGS IN THE DIATOM GENUS SKELETONEMA (BACILLARIOPHYTA) 1 , 2005 .

[60]  P. Qian,et al.  Vertical stratification of microbial communities in the Red Sea revealed by 16S rDNA pyrosequencing , 2011, The ISME Journal.

[61]  D. Vaulot,et al.  Composition of the summer photosynthetic pico and nanoplankton communities in the Beaufort Sea assessed by T-RFLP and sequences of the 18S rRNA gene from flow cytometry sorted samples , 2012, The ISME Journal.

[62]  D. Scanlan,et al.  Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). , 2008, Environmental microbiology.

[63]  N. Metzl,et al.  Red Sea budgets of salinity, nutrients and carbon calculated in the Strait of Bab-El-Mandab during the summer and winter seasons , 1989 .

[64]  D. Scanlan,et al.  Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean , 2013, The ISME Journal.

[65]  D. Vaulot,et al.  A Single Species, Micromonas pusilla (Prasinophyceae), Dominates the Eukaryotic Picoplankton in the Western English Channel , 2004, Applied and Environmental Microbiology.

[66]  D. Vaqué,et al.  Controls on planktonic metabolism in the Bay of Blanes, northwestern Mediterranean littoral , 2004 .

[67]  T. Gregory,et al.  The correlation between rDNA copy number and genome size in eukaryotes. , 2003, Genome.

[68]  I. Hewson,et al.  Temporal and spatial scales of variation in bacterioplankton assemblages of oligotrophic surface waters , 2006 .

[69]  S. Giovannoni,et al.  Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes , 2015, Science.

[70]  R. Burton,et al.  Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids , 2011, The ISME Journal.

[71]  A. Klindworth,et al.  Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies , 2012, Nucleic acids research.

[72]  F. Not,et al.  Ecology and Diversity of Picoeukaryotes , 2008 .

[73]  R. Burton,et al.  Seasonality and vertical structure of microbial communities in an ocean gyre , 2009, The ISME Journal.

[74]  M. Cheung,et al.  Composition and genetic diversity of picoeukaryotes in subtropical coastal waters as revealed by 454 pyrosequencing , 2010, The ISME Journal.

[75]  M. Vernet,et al.  Composition and biomass of phytoplankton assemblages in coastal Antarctic waters: a comparison of chemotaxonomic and microscopic analyses , 2003 .

[76]  W. Ludwig,et al.  SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB , 2007, Nucleic acids research.