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Adaptation of intertidal biofilm communities is driven by metal ion and oxidative stresses.

Zhang W, Wang Y, Lee OO, Tian R, Cao H, Gao Z, Li Y, Yu L, Xu Y, Qian PY - Sci Rep (2013)

Bottom Line: To understand how microbes in intertidal biofilms adapt to the stresses, the microbial metagenomes of biofilms from intertidal and subtidal zones were compared.The genes responsible for resistance to metal ion and oxidative stresses were enriched in both 6-day and 12-day intertidal biofilms, including genes associated with secondary metabolism, inorganic ion transport and metabolism, signal transduction and extracellular polymeric substance metabolism.We hypothesize that a complex signaling network is used for stress tolerance and propose a model illustrating the relationships between these functions and environmental metal ion concentrations and oxidative stresses.

View Article: PubMed Central - PubMed

Affiliation: 1] KAUST Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong SAR, China [2].

ABSTRACT
Marine organisms in intertidal zones are subjected to periodical fluctuations and wave activities. To understand how microbes in intertidal biofilms adapt to the stresses, the microbial metagenomes of biofilms from intertidal and subtidal zones were compared. The genes responsible for resistance to metal ion and oxidative stresses were enriched in both 6-day and 12-day intertidal biofilms, including genes associated with secondary metabolism, inorganic ion transport and metabolism, signal transduction and extracellular polymeric substance metabolism. In addition, these genes were more enriched in 12-day than 6-day intertidal biofilms. We hypothesize that a complex signaling network is used for stress tolerance and propose a model illustrating the relationships between these functions and environmental metal ion concentrations and oxidative stresses. These findings show that bacteria use diverse mechanisms to adapt to intertidal zones and indicate that the community structures of intertidal biofilms are modulated by metal ion and oxidative stresses.

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Schematic model of microbial reactions triggered by oxidative and metal ion stresses in intertidal biofilms.Stress signals activate signal transduction pathways within bacterial cells, resulting in transporter activation, secondary metabolism and EPS production.
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f5: Schematic model of microbial reactions triggered by oxidative and metal ion stresses in intertidal biofilms.Stress signals activate signal transduction pathways within bacterial cells, resulting in transporter activation, secondary metabolism and EPS production.

Mentions: In summary, findings from the present study elucidated the stresses that shape the community structures of intertidal biofilms compared with subtidal biofilms. We hypothesize that intertidal biofilm signaling regulators are activated by metal ion and oxidative stresses present in this highly variable environment. Subsequently, the expression of EPS, secondary metabolites and ion transporters may occur (Fig. 5). Thus, the community is shaped by the two stresses, and environmental selection causes differences between intertidal and subtidal biofilm structures, as supported by the enrichment of genes responsible for coping with the two stresses in the 12-I biofilm compared with the 6-I biofilm. The pursuit of nutrients may be considered to play a more important role in shaping community structure than stresses imposed by the changing environment, as some organisms in intertidal zones suffer from nutrient limitation47. However, genes encoding sugar metabolism enzymes were more strongly represented by reads in the intertidal biofilms, and energy-dependent ion transporters and pumps were highly abundant in intertidal biofilms, which indicated that energy-saving mechanisms were not used and nutrient deficiencies did not occur in intertidal biofilms. Thus, the enrichment for these sugar metabolism genes should be considered as an adaptive mechanism to environmental stress. In conclusion, adaptation of the intertidal biofilm community is produced by metal ion and oxidative stresses. There is evidence that secondary metabolites and bacterial cell-to-cell signaling mediate interactions between bacteria and eukaryotes. Therefore, in addition to stress tolerance, the enrichment for secondary metabolism and signal transduction genes might also explain why intertidal microbial biofilms are more attractive to eukaryotes for settlement. However, direct linkage between these phenomena is still lacking. Finally, because our conclusions are based on analysis of metagenomes from only one intertidal site, additional data from a broader range of sites and during different seasons are required to evaluate whether the present results occur consistently between intertidal and subtidal biofilms.


Adaptation of intertidal biofilm communities is driven by metal ion and oxidative stresses.

Zhang W, Wang Y, Lee OO, Tian R, Cao H, Gao Z, Li Y, Yu L, Xu Y, Qian PY - Sci Rep (2013)

Schematic model of microbial reactions triggered by oxidative and metal ion stresses in intertidal biofilms.Stress signals activate signal transduction pathways within bacterial cells, resulting in transporter activation, secondary metabolism and EPS production.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3822395&req=5

f5: Schematic model of microbial reactions triggered by oxidative and metal ion stresses in intertidal biofilms.Stress signals activate signal transduction pathways within bacterial cells, resulting in transporter activation, secondary metabolism and EPS production.
Mentions: In summary, findings from the present study elucidated the stresses that shape the community structures of intertidal biofilms compared with subtidal biofilms. We hypothesize that intertidal biofilm signaling regulators are activated by metal ion and oxidative stresses present in this highly variable environment. Subsequently, the expression of EPS, secondary metabolites and ion transporters may occur (Fig. 5). Thus, the community is shaped by the two stresses, and environmental selection causes differences between intertidal and subtidal biofilm structures, as supported by the enrichment of genes responsible for coping with the two stresses in the 12-I biofilm compared with the 6-I biofilm. The pursuit of nutrients may be considered to play a more important role in shaping community structure than stresses imposed by the changing environment, as some organisms in intertidal zones suffer from nutrient limitation47. However, genes encoding sugar metabolism enzymes were more strongly represented by reads in the intertidal biofilms, and energy-dependent ion transporters and pumps were highly abundant in intertidal biofilms, which indicated that energy-saving mechanisms were not used and nutrient deficiencies did not occur in intertidal biofilms. Thus, the enrichment for these sugar metabolism genes should be considered as an adaptive mechanism to environmental stress. In conclusion, adaptation of the intertidal biofilm community is produced by metal ion and oxidative stresses. There is evidence that secondary metabolites and bacterial cell-to-cell signaling mediate interactions between bacteria and eukaryotes. Therefore, in addition to stress tolerance, the enrichment for secondary metabolism and signal transduction genes might also explain why intertidal microbial biofilms are more attractive to eukaryotes for settlement. However, direct linkage between these phenomena is still lacking. Finally, because our conclusions are based on analysis of metagenomes from only one intertidal site, additional data from a broader range of sites and during different seasons are required to evaluate whether the present results occur consistently between intertidal and subtidal biofilms.

Bottom Line: To understand how microbes in intertidal biofilms adapt to the stresses, the microbial metagenomes of biofilms from intertidal and subtidal zones were compared.The genes responsible for resistance to metal ion and oxidative stresses were enriched in both 6-day and 12-day intertidal biofilms, including genes associated with secondary metabolism, inorganic ion transport and metabolism, signal transduction and extracellular polymeric substance metabolism.We hypothesize that a complex signaling network is used for stress tolerance and propose a model illustrating the relationships between these functions and environmental metal ion concentrations and oxidative stresses.

View Article: PubMed Central - PubMed

Affiliation: 1] KAUST Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong SAR, China [2].

ABSTRACT
Marine organisms in intertidal zones are subjected to periodical fluctuations and wave activities. To understand how microbes in intertidal biofilms adapt to the stresses, the microbial metagenomes of biofilms from intertidal and subtidal zones were compared. The genes responsible for resistance to metal ion and oxidative stresses were enriched in both 6-day and 12-day intertidal biofilms, including genes associated with secondary metabolism, inorganic ion transport and metabolism, signal transduction and extracellular polymeric substance metabolism. In addition, these genes were more enriched in 12-day than 6-day intertidal biofilms. We hypothesize that a complex signaling network is used for stress tolerance and propose a model illustrating the relationships between these functions and environmental metal ion concentrations and oxidative stresses. These findings show that bacteria use diverse mechanisms to adapt to intertidal zones and indicate that the community structures of intertidal biofilms are modulated by metal ion and oxidative stresses.

Show MeSH
Related in: MedlinePlus