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Emerging spatial patterns in Antarctic prokaryotes.

Chong CW, Pearce DA, Convey P - Front Microbiol (2015)

Bottom Line: Bacterial dispersal mechanisms and colonization patterns remain largely unaddressed, although evidence for regional evolutionary differentiation is rapidly accruing and, with this, there is increasing appreciation of patterns in regional bacterial biogeography in this large part of the globe.In this review, we set out to describe the state of knowledge of Antarctic prokaryote diversity patterns, drawing analogy with those of eukaryote groups where appropriate.Based on our synthesis, it is clear that spatial patterns of Antarctic prokaryotes can be unique at local scales, while the limited evidence available to date supports the group exhibiting overall regional biogeographical patterns similar to the eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences, School of Pharmacy, International Medical University, Kuala Lumpur Malaysia ; National Antarctic Research Center, University of Malaya, Kuala Lumpur Malaysia.

ABSTRACT
Recent advances in knowledge of patterns of biogeography in terrestrial eukaryotic organisms have led to a fundamental paradigm shift in understanding of the controls and history of life on land in Antarctica, and its interactions over the long term with the glaciological and geological processes that have shaped the continent. However, while it has long been recognized that the terrestrial ecosystems of Antarctica are dominated by microbes and their processes, knowledge of microbial diversity and distributions has lagged far behind that of the macroscopic eukaryote organisms. Increasing human contact with and activity in the continent is leading to risks of biological contamination and change in a region whose isolation has protected it for millions of years at least; these risks may be particularly acute for microbial communities which have, as yet, received scant recognition and attention. Even a matter apparently as straightforward as Protected Area designation in Antarctica requires robust biodiversity data which, in most parts of the continent, remain almost completely unavailable. A range of important contributing factors mean that it is now timely to reconsider the state of knowledge of Antarctic terrestrial prokaryotes. Rapid advances in molecular biological approaches are increasingly demonstrating that bacterial diversity in Antarctica may be far greater than previously thought, and that there is overlap in the environmental controls affecting both Antarctic prokaryotic and eukaryotic communities. Bacterial dispersal mechanisms and colonization patterns remain largely unaddressed, although evidence for regional evolutionary differentiation is rapidly accruing and, with this, there is increasing appreciation of patterns in regional bacterial biogeography in this large part of the globe. In this review, we set out to describe the state of knowledge of Antarctic prokaryote diversity patterns, drawing analogy with those of eukaryote groups where appropriate. Based on our synthesis, it is clear that spatial patterns of Antarctic prokaryotes can be unique at local scales, while the limited evidence available to date supports the group exhibiting overall regional biogeographical patterns similar to the eukaryotes. We further consider the applicability of the concept of "functional redundancy" for the Antarctic microbial community and highlight the requirements for proper consideration of their important and distinctive roles in Antarctic terrestrial ecosystems.

No MeSH data available.


Schematic illustration of an oligotroph’s response to alteration in local nutrient content. The oligotroph is suppressed periodically when large amounts of nutrients are available. Biomass then returns to the original level when the nutrients become depleted by the copiotroph, promoted by environmental change. In the event of prolonged nutrient alteration oligotrophs may drop below the biomass threshold (lower graph), and it will not recover even if nutrient levels returns to the original state.
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Figure 3: Schematic illustration of an oligotroph’s response to alteration in local nutrient content. The oligotroph is suppressed periodically when large amounts of nutrients are available. Biomass then returns to the original level when the nutrients become depleted by the copiotroph, promoted by environmental change. In the event of prolonged nutrient alteration oligotrophs may drop below the biomass threshold (lower graph), and it will not recover even if nutrient levels returns to the original state.

Mentions: Developing this concept further, and integrating the increasing reports of bacterial regionalization within the Antarctic (Yergeau et al., 2007b; Chong et al., 2013; Sokol et al., 2013), we propose here a new conceptual model to explain the mechanism underlying species-function relationships in Antarctica. The Antarctic soil ecosystem is supported by a highly diverse but region-specific bacterial community. For instance, nutrient-rich (e.g., penguin rookeries) and nutrient-poor (e.g., barren soil) environments from different Antarctic regions contain both copiotrophs (high nutrient requirement, e.g., Flavobacterium spp.) and oligotrophs (low nutrient requirement, e.g., Acidobacterium spp.; Fierer et al., 2007; Aislabie et al., 2008; Chong et al., 2010; Bottos et al., 2014a). Soil samples obtained across different regions exhibit distinct community memberships with reference to these groups, but the phylogenetic similarity of their members is greater within the same biogeographic region than it is between regions (Figure 2, comparing upper and lower panels). In any particular system, the biomass of the copiotrophs and oligotrophs is dependent on the ecological characteristics of the habitat present. Nutrient-poor habitats host a greater percentage of oligotrophs such as Acidobacteria that convert recalcitrant carbon such as xylan (from autotrophs) and pectin (from wind-blown plant materials) into labile carbon (Bokhorst et al., 2007; Ward et al., 2009), while copiotrophs such as some Bacteroidetes dominate nutrient-rich sites, degrading the available high molecular weight organic carbon (Zdanowski et al., 2005; Aislabie et al., 2008; Chong et al., 2010). Changes in local environmental conditions, such as deposition of nutrients through aeolian transfer, or loss through leaching, can trigger rapid community turnover to match the new functional requirement (Saul et al., 2005; Barrett et al., 2006a; Tiao et al., 2012; Dennis et al., 2013; Figure 2). If such community compositional shifts involve specialists (rare species with unique traits) being lost or reduced below a critical biomass level, this may become a limiting factor in responding to subsequent changes (Figure 3).


Emerging spatial patterns in Antarctic prokaryotes.

Chong CW, Pearce DA, Convey P - Front Microbiol (2015)

Schematic illustration of an oligotroph’s response to alteration in local nutrient content. The oligotroph is suppressed periodically when large amounts of nutrients are available. Biomass then returns to the original level when the nutrients become depleted by the copiotroph, promoted by environmental change. In the event of prolonged nutrient alteration oligotrophs may drop below the biomass threshold (lower graph), and it will not recover even if nutrient levels returns to the original state.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4588704&req=5

Figure 3: Schematic illustration of an oligotroph’s response to alteration in local nutrient content. The oligotroph is suppressed periodically when large amounts of nutrients are available. Biomass then returns to the original level when the nutrients become depleted by the copiotroph, promoted by environmental change. In the event of prolonged nutrient alteration oligotrophs may drop below the biomass threshold (lower graph), and it will not recover even if nutrient levels returns to the original state.
Mentions: Developing this concept further, and integrating the increasing reports of bacterial regionalization within the Antarctic (Yergeau et al., 2007b; Chong et al., 2013; Sokol et al., 2013), we propose here a new conceptual model to explain the mechanism underlying species-function relationships in Antarctica. The Antarctic soil ecosystem is supported by a highly diverse but region-specific bacterial community. For instance, nutrient-rich (e.g., penguin rookeries) and nutrient-poor (e.g., barren soil) environments from different Antarctic regions contain both copiotrophs (high nutrient requirement, e.g., Flavobacterium spp.) and oligotrophs (low nutrient requirement, e.g., Acidobacterium spp.; Fierer et al., 2007; Aislabie et al., 2008; Chong et al., 2010; Bottos et al., 2014a). Soil samples obtained across different regions exhibit distinct community memberships with reference to these groups, but the phylogenetic similarity of their members is greater within the same biogeographic region than it is between regions (Figure 2, comparing upper and lower panels). In any particular system, the biomass of the copiotrophs and oligotrophs is dependent on the ecological characteristics of the habitat present. Nutrient-poor habitats host a greater percentage of oligotrophs such as Acidobacteria that convert recalcitrant carbon such as xylan (from autotrophs) and pectin (from wind-blown plant materials) into labile carbon (Bokhorst et al., 2007; Ward et al., 2009), while copiotrophs such as some Bacteroidetes dominate nutrient-rich sites, degrading the available high molecular weight organic carbon (Zdanowski et al., 2005; Aislabie et al., 2008; Chong et al., 2010). Changes in local environmental conditions, such as deposition of nutrients through aeolian transfer, or loss through leaching, can trigger rapid community turnover to match the new functional requirement (Saul et al., 2005; Barrett et al., 2006a; Tiao et al., 2012; Dennis et al., 2013; Figure 2). If such community compositional shifts involve specialists (rare species with unique traits) being lost or reduced below a critical biomass level, this may become a limiting factor in responding to subsequent changes (Figure 3).

Bottom Line: Bacterial dispersal mechanisms and colonization patterns remain largely unaddressed, although evidence for regional evolutionary differentiation is rapidly accruing and, with this, there is increasing appreciation of patterns in regional bacterial biogeography in this large part of the globe.In this review, we set out to describe the state of knowledge of Antarctic prokaryote diversity patterns, drawing analogy with those of eukaryote groups where appropriate.Based on our synthesis, it is clear that spatial patterns of Antarctic prokaryotes can be unique at local scales, while the limited evidence available to date supports the group exhibiting overall regional biogeographical patterns similar to the eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences, School of Pharmacy, International Medical University, Kuala Lumpur Malaysia ; National Antarctic Research Center, University of Malaya, Kuala Lumpur Malaysia.

ABSTRACT
Recent advances in knowledge of patterns of biogeography in terrestrial eukaryotic organisms have led to a fundamental paradigm shift in understanding of the controls and history of life on land in Antarctica, and its interactions over the long term with the glaciological and geological processes that have shaped the continent. However, while it has long been recognized that the terrestrial ecosystems of Antarctica are dominated by microbes and their processes, knowledge of microbial diversity and distributions has lagged far behind that of the macroscopic eukaryote organisms. Increasing human contact with and activity in the continent is leading to risks of biological contamination and change in a region whose isolation has protected it for millions of years at least; these risks may be particularly acute for microbial communities which have, as yet, received scant recognition and attention. Even a matter apparently as straightforward as Protected Area designation in Antarctica requires robust biodiversity data which, in most parts of the continent, remain almost completely unavailable. A range of important contributing factors mean that it is now timely to reconsider the state of knowledge of Antarctic terrestrial prokaryotes. Rapid advances in molecular biological approaches are increasingly demonstrating that bacterial diversity in Antarctica may be far greater than previously thought, and that there is overlap in the environmental controls affecting both Antarctic prokaryotic and eukaryotic communities. Bacterial dispersal mechanisms and colonization patterns remain largely unaddressed, although evidence for regional evolutionary differentiation is rapidly accruing and, with this, there is increasing appreciation of patterns in regional bacterial biogeography in this large part of the globe. In this review, we set out to describe the state of knowledge of Antarctic prokaryote diversity patterns, drawing analogy with those of eukaryote groups where appropriate. Based on our synthesis, it is clear that spatial patterns of Antarctic prokaryotes can be unique at local scales, while the limited evidence available to date supports the group exhibiting overall regional biogeographical patterns similar to the eukaryotes. We further consider the applicability of the concept of "functional redundancy" for the Antarctic microbial community and highlight the requirements for proper consideration of their important and distinctive roles in Antarctic terrestrial ecosystems.

No MeSH data available.