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Biogeography, Cultivation and Genomic Characterization of Prochlorococcus in the Red Sea

Aquatic primary productivity mainly depends on pelagic phytoplankton.
The globally abundant marine picocyanobacteria Prochlorococcus comprises a
significant fraction of the photosynthetic biomass in most tropical, oligotrophic
oceans. The Red Sea is an enclosed narrow body of water characterized by
continuous solar irradiance, and negligible annual rainfall, in addition to elevated
temperatures and salinity levels, which mimics a global warming scenario.
Analysis of 16S rRNA sequences of bacterioplankton communities indicated the
predominance of a high-light adapted ecotype (HL II) of Prochlorococcus at the
surface of the Northern and Central Red Sea. To this end, we analyzed the
distribution of Prochlorococcus at multiple depths within and below the euphotic
zone in different regions of the Red Sea, using clone libraries of the 16S–23S
rRNA internal transcribed spacer (ITS) region. Results indicated a high diversity
of Prochlorococcus ecotypes at the 100 m depth in the water column and an
unusual dominance of HL II-related sequences in deeper waters of the Red Sea.
To further investigate the microdiversity of Prochlorococcus over a wider
biogeographical scope, we used a 454-pyrosequencing approach to analyze
rpoC1 gene pyrotags. Samples were collected from the surface of the water
column to up to 500 m at 45 stations that span the Red Sea’s main basin from
4
north to south. Phylogenetic analysis of abundant rpoC1 OTUs revealed
genotypes of recently discovered strains that belong to the high-light and lowlight
clades. In addition, we used a rapid community-profiling tool (GraftM) and
quantitatively analyzed rpoC1 gene abundance from 45 metagenomes to assess
the Prochlorococcus community structure across vertical and horizontal
physicochemical gradients. Results revealed the clustering of samples according
to their depth and a strong influence on ecotypic distribution by temperature and
oxygen levels. In efforts to better understand how the cells survive the unusual
features of the Red Sea, a Prochlorococcus strain of the HL II adapted clade
from the euphotic zone was cultured, enabling morphological analyses and
growth rates measurements for the strain. In addition, we successfully
sequenced and annotated the genome of the strain, which was then used for
genomic comparison with other ecotypes. Interestingly, the set of unique genes
identified in the draft genome included genes encoding proteins involved in salt
tolerance mechanisms. The expression level and pattern of these genes in the
Red Sea water column was explored through metatranscriptomic mapping and
revealed their occurrence throughout, independent of the diel cycle. This led to
the hypothesis that Prochlorococcus populations in the highly saline Red Sea are
able to biosynthesize additional compatible solutes via several pathways to
counterbalance the effects of salt stress. The results presented in this
dissertation provide the first glimpse on how the environmental parameters of the
Red Sea can affect the evolution, diversity and distribution patterns of
Prochlorococcus ecotypes.

Identiferoai:union.ndltd.org:kaust.edu.sa/oai:repository.kaust.edu.sa:10754/584234
Date16 December 2015
CreatorsShibl, Ahmed A.
ContributorsStingl, Ulrich, Biological and Environmental Sciences and Engineering (BESE) Division, Moran, Xose Anxelu G., Pain, Arnab, Siam, Rania
Source SetsKing Abdullah University of Science and Technology
LanguageEnglish
Detected LanguageEnglish
TypeDissertation
Rights2016-12-18, At the time of archiving, the student author of this dissertation opted to temporarily restrict access to it. The full text of this dissertation became available to the public after the expiration of the embargo on 2016-12-18.

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