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Is Proteorhodopsin a general light-driven stress adaptation system for survival in cold environments

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Feng, Shi (2014) Is Proteorhodopsin a general light-driven stress adaptation system for survival in cold environments. PhD thesis, University of Tasmania.

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Abstract

This study aimed to achieve a better understanding of microbial adaptations in sea ice
focusing on the physiological role of the light harvesting proton pump
proteorhodopsin. To carry out these aims the research mainly focused on exploring the
genome biology, physiology and life strategy of the model sea-ice bacterial species
Psychroflexus torquis, an extremely psychrophilic member of the family
Flavobacteriaceae (phylum Bacteroidetes). P. torquis has a bipolar distribution and is
only known to occur in polar sea-ice and associated polar waters. It possesses
proteorhodopsin and is believed to have a predominantly epiphytic lifestyle, mainly
dwelling on sea-ice diatoms in sea-ice basal assemblages. This study extensively used gel-free label-free based proteomic approach to explore P. torquis’ genome biology
and unravel the role of proteorhodopsin in aiding the species adaptation to the
extreme sea ice environment. Sea ice has been estimated to have only become a stable feature on Earth in the last
few million years ago thus it has been hypothesized that bacteria adapted to sea-ice
acquired or exchange survival traits via horizontal gene transfer (HGT) between other
sea ice dwelling microorganisms relatively recently. To examine the question whether
sea-ice bacteria, such as P. torquis are endemic and display sea ice-ecosystem
specialism a comparison of P. torquis’ genome to its very closely related (99% 16S
rRNA gene sequence similarity) sister species, P. gondwanensis ACAM 44T, which is
only known to dwell in Antarctic hypersaline lakes, was performed. This comparison allowed for the determination of the level of HGT, what traits show evidence of HGT,
what traits are relevant to the sea-ice ecosystem, and whether these genes are highly
expressed, which would be indicative of their biological importance to P. torquis. The
results show that in P. torquis ATCC 700755T (genome size 4.3 Mbp) HGT has
occurred much more extensively compared to P. gondwanensis (genome size 3.3 Mbp)
and genetic features that can be linked as a sea ice specific adaptation are mainly
concentrated on numerous genomic islands absent from P. gondwanensis. Genes
encoding sea-ice ecosystem relevant traits, such as secreted exopolysaccharide,
poly-unsaturated fatty acids, and ice binding proteins, form gene clusters on a number
of these genomic islands. Proteomic analysis revealed that the encoded proteins for
many sea-ice relevant traits are highly abundant under standard laboratory growth
conditions. The genomic islands feature comparatively low gene density, a high
concentration of pseudogenes, repetitive genetic elements, and addiction modules,
indicative of large scale HGT either via phage or conjugation driven insertions.The
overall results suggest the extensive level and nature of gene acquisition in P. torquis
indicates its potential evolution to sea-ice ecosystem specialism. In that respect P.
torquis seems to be an excellent model to study sea-ice functional biology. The initial
screening of the P. torquis ATCC 700755T genome revealed the presence of a
proteorhodopsin gene. Previous studies have demonstrated proteorhodopsin-based
phototrophy can enhance bacterial growth and survival during nutrient-stress
conditions. But proteorhodopsins are widespread in natural environments and these
environments may have other stress conditions for which proteorhodopsin can be advantageous. So it can be hypothesized that proteorhodopsin may provide
growth/survival advantage under stress conditions that are associated with a specific
econiche. Growth studies on proteorhodopsin-containing P. torquis have demonstrated
for the first time that light-stimulated growth can be linked to salinity stress rather
than nutrient limitation. In addition, proteorhodopsin abundance and associated
proton-pumping ability is also salinity dependent. The results extend the existing
hypothesis that light can provide energy for marine prokaryotes through
proteorhodopsin under stress conditions other than nutrient stress. To gain a deeper insight into the physiological role of proteorhodopsin and the life
strategy of P. torquis, a gel-free label-free quantitative proteomic approach was used.
Proteome analysis revealed how P. torquis responded to different salinity and
illumination levels by regulating its energy generation, nutrient uptake transporters,
adhesion ability and gliding motility. The protein expression patterns of P. torquis
indicates that it can use light to gain an advantage in colonizing phytoplanktonic
surfaces, taking up more nutrients, and optimizing energy production. This study
provided a comprehensive understanding of life style in sea ice and also partly
revealed the physiological role of proteorhodopsin and its complex interrelationships.

Item Type: Thesis (PhD)
Keywords: Proteorhodopsin, sea-ice, proteomic, comparative geomics, evolution, life strategy
Copyright Holders: Copyright the Author
Copyright Information:

Copyright 2014 the Author

Date Deposited: 27 May 2015 02:42
Last Modified: 11 Nov 2016 16:00
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