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Differential utilization patterns of dissolved organic phosphorus compounds by heterotrophic bacteria in two mountain lakes

View Article: PubMed Central - PubMed

ABSTRACT

Although phosphorus limitation is common in freshwaters and bacteria are known to use dissolved organic phosphorus (DOP), little is known about how efficiently DOP compounds are taken up by individual bacterial taxa. Here, we assessed bacterial uptake of three model DOP substrates in two mountain lakes and examined whether DOP uptake followed concentration-dependent patterns. We determined bulk uptake rates by the bacterioplankton and examined bacterial taxon-specific substrate uptake patterns using microautoradiography combined with catalyzed reporter deposition–fluorescence in situ hybridization. Our results show that in the oligotrophic alpine lake, bacteria took up ATP, glucose-6-phosphate and glycerol-3-phosphate to similar extents (mean 29.7 ± 4.3% Bacteria), whereas in the subalpine mesotrophic lake, ca. 40% of bacteria took up glucose-6-phosphate, but only ∼20% took up ATP or glycerol-3-phosphate. In both lakes, the R-BT cluster of Betaproteobacteria (lineage of genus Limnohabitans) was over-represented in glucose-6-phosphate and glycerol-3-phosphate uptake, whereas AcI Actinobacteria were under-represented in the uptake of those substrates. Alphaproteobacteria and Bacteroidetes contributed to DOP uptake proportionally to their in situ abundance. Our results demonstrate that R-BT Betaproteobacteria are the most active bacteria in DOP acquisition, whereas the abundant AcI Actinobacteria may either lack high affinity DOP uptake systems or have reduced phosphorus requirements.

No MeSH data available.


The contribution of Betaproteobacteria (dark blue) and its R-BT cluster (light blue), Bacteroidetes (green), Alphaproteobacteria (orange), and AcI Actinobacteria (red) to ATP, glucose-6-phosphate and glycerol-3-phosphate uptake plotted against their contribution to abundance in GKS (A) and PIB (B). The 1:1 line indicates that the contribution of a bacterial group to substrate uptake equals its contribution to bacterial abundance. Circle and triangle indicate the epilimnion and hypolimnion, respectively. Different substrate concentrations are given by symbol size: small, 0.2 nM; medium, 1 nM; large, 5 nM. Values are the mean of triplicate samples.
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fig3: The contribution of Betaproteobacteria (dark blue) and its R-BT cluster (light blue), Bacteroidetes (green), Alphaproteobacteria (orange), and AcI Actinobacteria (red) to ATP, glucose-6-phosphate and glycerol-3-phosphate uptake plotted against their contribution to abundance in GKS (A) and PIB (B). The 1:1 line indicates that the contribution of a bacterial group to substrate uptake equals its contribution to bacterial abundance. Circle and triangle indicate the epilimnion and hypolimnion, respectively. Different substrate concentrations are given by symbol size: small, 0.2 nM; medium, 1 nM; large, 5 nM. Values are the mean of triplicate samples.

Mentions: The contribution of a bacterial group to the uptake of ATP, Glu6P and Gly3P versus its contribution to bacterial abundance differed depending on the substrate and lake considered (Fig. 3A and B). Alphaproteobacteria usually contributed to the uptake of the three DOP compounds proportionally to their in situ abundance, though they were slightly over-represented in the uptake of ATP in the epilimnion of both lakes. Betaproteobacteria and its R-BT cluster were significantly over-represented in the uptake of Glu6P and Gly3P as compared with their in situ abundance in GKS (ANOVA, P < 0.01), whereas their contribution to ATP incorporation was proportional to their abundance. Similarly in PIB, they were close to the 1:1 line for ATP and Glu6P uptake, but were over-represented for Gly3P (ANOVA, P < 0.05). Bacteroidetes contributed to substrate incorporation in relation to their relative abundance, except in GKS where they were slightly under-represented in the uptake of Glu6P and Gly3P. AcI Actinobacteria were poorly represented in the uptake of Glu6P and Gly3P. This trend was significantly more pronounced in GKS than in PIB (t-test, P < 0.001). Their contribution to ATP uptake was rather close to the 1:1 line in both lakes (Fig. 3).


Differential utilization patterns of dissolved organic phosphorus compounds by heterotrophic bacteria in two mountain lakes
The contribution of Betaproteobacteria (dark blue) and its R-BT cluster (light blue), Bacteroidetes (green), Alphaproteobacteria (orange), and AcI Actinobacteria (red) to ATP, glucose-6-phosphate and glycerol-3-phosphate uptake plotted against their contribution to abundance in GKS (A) and PIB (B). The 1:1 line indicates that the contribution of a bacterial group to substrate uptake equals its contribution to bacterial abundance. Circle and triangle indicate the epilimnion and hypolimnion, respectively. Different substrate concentrations are given by symbol size: small, 0.2 nM; medium, 1 nM; large, 5 nM. Values are the mean of triplicate samples.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4940451&req=5

fig3: The contribution of Betaproteobacteria (dark blue) and its R-BT cluster (light blue), Bacteroidetes (green), Alphaproteobacteria (orange), and AcI Actinobacteria (red) to ATP, glucose-6-phosphate and glycerol-3-phosphate uptake plotted against their contribution to abundance in GKS (A) and PIB (B). The 1:1 line indicates that the contribution of a bacterial group to substrate uptake equals its contribution to bacterial abundance. Circle and triangle indicate the epilimnion and hypolimnion, respectively. Different substrate concentrations are given by symbol size: small, 0.2 nM; medium, 1 nM; large, 5 nM. Values are the mean of triplicate samples.
Mentions: The contribution of a bacterial group to the uptake of ATP, Glu6P and Gly3P versus its contribution to bacterial abundance differed depending on the substrate and lake considered (Fig. 3A and B). Alphaproteobacteria usually contributed to the uptake of the three DOP compounds proportionally to their in situ abundance, though they were slightly over-represented in the uptake of ATP in the epilimnion of both lakes. Betaproteobacteria and its R-BT cluster were significantly over-represented in the uptake of Glu6P and Gly3P as compared with their in situ abundance in GKS (ANOVA, P < 0.01), whereas their contribution to ATP incorporation was proportional to their abundance. Similarly in PIB, they were close to the 1:1 line for ATP and Glu6P uptake, but were over-represented for Gly3P (ANOVA, P < 0.05). Bacteroidetes contributed to substrate incorporation in relation to their relative abundance, except in GKS where they were slightly under-represented in the uptake of Glu6P and Gly3P. AcI Actinobacteria were poorly represented in the uptake of Glu6P and Gly3P. This trend was significantly more pronounced in GKS than in PIB (t-test, P < 0.001). Their contribution to ATP uptake was rather close to the 1:1 line in both lakes (Fig. 3).

View Article: PubMed Central - PubMed

ABSTRACT

Although phosphorus limitation is common in freshwaters and bacteria are known to use dissolved organic phosphorus (DOP), little is known about how efficiently DOP compounds are taken up by individual bacterial taxa. Here, we assessed bacterial uptake of three model DOP substrates in two mountain lakes and examined whether DOP uptake followed concentration-dependent patterns. We determined bulk uptake rates by the bacterioplankton and examined bacterial taxon-specific substrate uptake patterns using microautoradiography combined with catalyzed reporter deposition&ndash;fluorescence in situ hybridization. Our results show that in the oligotrophic alpine lake, bacteria took up ATP, glucose-6-phosphate and glycerol-3-phosphate to similar extents (mean 29.7 &plusmn; 4.3% Bacteria), whereas in the subalpine mesotrophic lake, ca. 40% of bacteria took up glucose-6-phosphate, but only &sim;20% took up ATP or glycerol-3-phosphate. In both lakes, the R-BT cluster of Betaproteobacteria (lineage of genus Limnohabitans) was over-represented in glucose-6-phosphate and glycerol-3-phosphate uptake, whereas AcI Actinobacteria were under-represented in the uptake of those substrates. Alphaproteobacteria and Bacteroidetes contributed to DOP uptake proportionally to their in situ abundance. Our results demonstrate that R-BT Betaproteobacteria are the most active bacteria in DOP acquisition, whereas the abundant AcI Actinobacteria may either lack high affinity DOP uptake systems or have reduced phosphorus requirements.

No MeSH data available.