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Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment.

Thomas T, Evans FF, Schleheck D, Mai-Prochnow A, Burke C, Penesyan A, Dalisay DS, Stelzer-Braid S, Saunders N, Johnson J, Ferriera S, Kjelleberg S, Egan S - PLoS ONE (2008)

Bottom Line: To gain a broader understanding into the adaptation to a surface-associated life-style, we have sequenced and analysed the genome of P. tunicata and compared it to the genomes of closely related strains.We found that the P. tunicata genome contains several genes and gene clusters that are involved in the production of inhibitory compounds against surface competitors and secondary colonisers.The genome analysis has revealed several physiological features that would provide P. tunciata with competitive advantage against other members of the surface-associated community.

View Article: PubMed Central - PubMed

Affiliation: Centre of Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, New South Wales, Australia. t.thomas@unsw.edu.au

ABSTRACT

Background: Colonisation of sessile eukaryotic host surfaces (e.g. invertebrates and seaweeds) by bacteria is common in the marine environment and is expected to create significant inter-species competition and other interactions. The bacterium Pseudoalteromonas tunicata is a successful competitor on marine surfaces owing primarily to its ability to produce a number of inhibitory molecules. As such P. tunicata has become a model organism for the studies into processes of surface colonisation and eukaryotic host-bacteria interactions.

Methodology/principal findings: To gain a broader understanding into the adaptation to a surface-associated life-style, we have sequenced and analysed the genome of P. tunicata and compared it to the genomes of closely related strains. We found that the P. tunicata genome contains several genes and gene clusters that are involved in the production of inhibitory compounds against surface competitors and secondary colonisers. Features of P. tunicata's oxidative stress response, iron scavenging and nutrient acquisition show that the organism is well adapted to high-density communities on surfaces. Variation of the P. tunicata genome is suggested by several landmarks of genetic rearrangements and mobile genetic elements (e.g. transposons, CRISPRs, phage). Surface attachment is likely to be mediated by curli, novel pili, a number of extracellular polymers and potentially other unexpected cell surface proteins. The P. tunicata genome also shows a utilisation pattern of extracellular polymers that would avoid a degradation of its recognised hosts, while potentially causing detrimental effects on other host types. In addition, the prevalence of recognised virulence genes suggests that P. tunicata has the potential for pathogenic interactions.

Conclusions/significance: The genome analysis has revealed several physiological features that would provide P. tunciata with competitive advantage against other members of the surface-associated community. We have also identified properties that could mediate interactions with surfaces other than its currently recognised hosts. This together with the detection of known virulence genes leads to the hypothesis that P. tunicata maintains a carefully regulated balance between beneficial and detrimental interactions with a range of host surfaces.

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Functional comparison of Pseudoalteromonas and Alteromonas genomes.Relative abundance compared to all COGs (panel A) and absolute number of categories (panel B) for selected Pseudoalteromonas and Alteromonas species. COGs were extracted from IMG using greater than 30% identity and expectancy values of less than 10−5 cut-offs and assigned to functional categories.
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pone-0003252-g002: Functional comparison of Pseudoalteromonas and Alteromonas genomes.Relative abundance compared to all COGs (panel A) and absolute number of categories (panel B) for selected Pseudoalteromonas and Alteromonas species. COGs were extracted from IMG using greater than 30% identity and expectancy values of less than 10−5 cut-offs and assigned to functional categories.

Mentions: Hierarchical clustering and principle component analysis of cluster of orthologous groups (COG) with other sequenced members of the Alteromonadales available in the IMG database indicate that P. tunicata is functionally most closely related to P. haloplanktis, P. atlantica, Alteromonas macleodii and Alteromonadales sp. TW7. General features of these genomes are given in Table 1 and their phylogenetic relationship based on the 16S rRNA gene is illustrated in Figure 1. The COG profiles between these organisms revealed however a number of COG categories that were over-represented in P. tunicata (Figure 2) including signal transduction mechanisms, defence mechanisms and cell motility. P. tunicata shows the highest proportion of genes assigned to signal transduction (10.05%) of any Alteromondales genome (second highest: Shewanella amazonensis with 8.62%; lowest: Psychromonas sp. CMPT3 with 5.10%). This trend is mainly caused by an over-representation of COG5000 (signal transduction histidine kinase involved in nitrogen fixation and metabolism regulation) and COG0664 (cAMP-binding proteins - catabolite gene activator and regulatory subunit of cAMP-dependent protein kinases). P. tunicata also has the highest value (2.4%) for the COG category defence of any Alteromondales genome and this is specifically due to more genes related to ABC transporter functions, including those predicted to be involved in transport of drugs and/ or antimicrobial peptides (COG0577, COG1131, COG1136, COG1566) and those related to the synthesis of potential bioactive compounds such as non-ribosomal peptide synthetase (NRPS) modules (COG1020). The abundance of genes involved in transport and expression of potential defence compounds are consistent with P. tunicata's successful competition on living surfaces. The major difference in the COG category cell motility is in COG0840 (methyl-accepting chemotaxis protein), where P. tunicata has 35 hits, which is at least twice as many as any other Pseudoalteromonas or Alteromononas species.


Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment.

Thomas T, Evans FF, Schleheck D, Mai-Prochnow A, Burke C, Penesyan A, Dalisay DS, Stelzer-Braid S, Saunders N, Johnson J, Ferriera S, Kjelleberg S, Egan S - PLoS ONE (2008)

Functional comparison of Pseudoalteromonas and Alteromonas genomes.Relative abundance compared to all COGs (panel A) and absolute number of categories (panel B) for selected Pseudoalteromonas and Alteromonas species. COGs were extracted from IMG using greater than 30% identity and expectancy values of less than 10−5 cut-offs and assigned to functional categories.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2536512&req=5

pone-0003252-g002: Functional comparison of Pseudoalteromonas and Alteromonas genomes.Relative abundance compared to all COGs (panel A) and absolute number of categories (panel B) for selected Pseudoalteromonas and Alteromonas species. COGs were extracted from IMG using greater than 30% identity and expectancy values of less than 10−5 cut-offs and assigned to functional categories.
Mentions: Hierarchical clustering and principle component analysis of cluster of orthologous groups (COG) with other sequenced members of the Alteromonadales available in the IMG database indicate that P. tunicata is functionally most closely related to P. haloplanktis, P. atlantica, Alteromonas macleodii and Alteromonadales sp. TW7. General features of these genomes are given in Table 1 and their phylogenetic relationship based on the 16S rRNA gene is illustrated in Figure 1. The COG profiles between these organisms revealed however a number of COG categories that were over-represented in P. tunicata (Figure 2) including signal transduction mechanisms, defence mechanisms and cell motility. P. tunicata shows the highest proportion of genes assigned to signal transduction (10.05%) of any Alteromondales genome (second highest: Shewanella amazonensis with 8.62%; lowest: Psychromonas sp. CMPT3 with 5.10%). This trend is mainly caused by an over-representation of COG5000 (signal transduction histidine kinase involved in nitrogen fixation and metabolism regulation) and COG0664 (cAMP-binding proteins - catabolite gene activator and regulatory subunit of cAMP-dependent protein kinases). P. tunicata also has the highest value (2.4%) for the COG category defence of any Alteromondales genome and this is specifically due to more genes related to ABC transporter functions, including those predicted to be involved in transport of drugs and/ or antimicrobial peptides (COG0577, COG1131, COG1136, COG1566) and those related to the synthesis of potential bioactive compounds such as non-ribosomal peptide synthetase (NRPS) modules (COG1020). The abundance of genes involved in transport and expression of potential defence compounds are consistent with P. tunicata's successful competition on living surfaces. The major difference in the COG category cell motility is in COG0840 (methyl-accepting chemotaxis protein), where P. tunicata has 35 hits, which is at least twice as many as any other Pseudoalteromonas or Alteromononas species.

Bottom Line: To gain a broader understanding into the adaptation to a surface-associated life-style, we have sequenced and analysed the genome of P. tunicata and compared it to the genomes of closely related strains.We found that the P. tunicata genome contains several genes and gene clusters that are involved in the production of inhibitory compounds against surface competitors and secondary colonisers.The genome analysis has revealed several physiological features that would provide P. tunciata with competitive advantage against other members of the surface-associated community.

View Article: PubMed Central - PubMed

Affiliation: Centre of Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, New South Wales, Australia. t.thomas@unsw.edu.au

ABSTRACT

Background: Colonisation of sessile eukaryotic host surfaces (e.g. invertebrates and seaweeds) by bacteria is common in the marine environment and is expected to create significant inter-species competition and other interactions. The bacterium Pseudoalteromonas tunicata is a successful competitor on marine surfaces owing primarily to its ability to produce a number of inhibitory molecules. As such P. tunicata has become a model organism for the studies into processes of surface colonisation and eukaryotic host-bacteria interactions.

Methodology/principal findings: To gain a broader understanding into the adaptation to a surface-associated life-style, we have sequenced and analysed the genome of P. tunicata and compared it to the genomes of closely related strains. We found that the P. tunicata genome contains several genes and gene clusters that are involved in the production of inhibitory compounds against surface competitors and secondary colonisers. Features of P. tunicata's oxidative stress response, iron scavenging and nutrient acquisition show that the organism is well adapted to high-density communities on surfaces. Variation of the P. tunicata genome is suggested by several landmarks of genetic rearrangements and mobile genetic elements (e.g. transposons, CRISPRs, phage). Surface attachment is likely to be mediated by curli, novel pili, a number of extracellular polymers and potentially other unexpected cell surface proteins. The P. tunicata genome also shows a utilisation pattern of extracellular polymers that would avoid a degradation of its recognised hosts, while potentially causing detrimental effects on other host types. In addition, the prevalence of recognised virulence genes suggests that P. tunicata has the potential for pathogenic interactions.

Conclusions/significance: The genome analysis has revealed several physiological features that would provide P. tunciata with competitive advantage against other members of the surface-associated community. We have also identified properties that could mediate interactions with surfaces other than its currently recognised hosts. This together with the detection of known virulence genes leads to the hypothesis that P. tunicata maintains a carefully regulated balance between beneficial and detrimental interactions with a range of host surfaces.

Show MeSH