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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.


Bar charts representing the percentage of Bacteria, the R-BT cluster of Betaproteobacteria and the AcI lineage of Actinobacteria (as % hybridized cells) taking up ATP, glucose-6-phosphate and glycerol-3-phosphate at the three concentrations added (0.2, 1, 5 nM) in the epilimnion (open bars) and hypolimnion (filled bars) of GKS (A, C, E) and PIB (B, D, F). Values are the mean of triplicate incubations ±1 SD. Asterisks indicate significant changes in active cells due to increasing substrate concentrations. Data points above the bars represent the mean bulk substrate uptake rates determined from duplicate incubations ±1 SD.
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fig2: Bar charts representing the percentage of Bacteria, the R-BT cluster of Betaproteobacteria and the AcI lineage of Actinobacteria (as % hybridized cells) taking up ATP, glucose-6-phosphate and glycerol-3-phosphate at the three concentrations added (0.2, 1, 5 nM) in the epilimnion (open bars) and hypolimnion (filled bars) of GKS (A, C, E) and PIB (B, D, F). Values are the mean of triplicate incubations ±1 SD. Asterisks indicate significant changes in active cells due to increasing substrate concentrations. Data points above the bars represent the mean bulk substrate uptake rates determined from duplicate incubations ±1 SD.

Mentions: The examined bacterial groups exhibited substrate-specific uptake patterns that were similar in both lakes (Fig. 1A and B). Betaproteobacteria and its R-BT cluster yielded the highest proportions of cells taking up Glu6P and Gly3P in the lakes, though more cells were labeled positive in GKS than in PIB. For both groups, the proportions of cells positive for ATP uptake represented ca. 20% of hybridized cells. Bacteroidetes and AcI Actinobacteria showed similar Glu6P and Gly3P uptake patterns (Fig. 1) and were often different from those of other bacterial groups (ANOVA, P < 0.01). In general, AcI Actinobacteria was weakly represented in the uptake of any substrate (range: ∼6–22% of hybridized cells) with the exception of Glu6P in PIB (range: ∼19–32% of hybridized cells; Figs 1B and 2F). By contrast, more Bacteroidetes cells were labeled positive for ATP uptake (22–36%) than for Gly3P or Glu6P uptake in the lakes. Around 30–55% of Alphaproteobacteria incorporated ATP and Gly3P (hypolimnion) in GKS and Glu6P in PIB.


Differential utilization patterns of dissolved organic phosphorus compounds by heterotrophic bacteria in two mountain lakes
Bar charts representing the percentage of Bacteria, the R-BT cluster of Betaproteobacteria and the AcI lineage of Actinobacteria (as % hybridized cells) taking up ATP, glucose-6-phosphate and glycerol-3-phosphate at the three concentrations added (0.2, 1, 5 nM) in the epilimnion (open bars) and hypolimnion (filled bars) of GKS (A, C, E) and PIB (B, D, F). Values are the mean of triplicate incubations ±1 SD. Asterisks indicate significant changes in active cells due to increasing substrate concentrations. Data points above the bars represent the mean bulk substrate uptake rates determined from duplicate incubations ±1 SD.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

fig2: Bar charts representing the percentage of Bacteria, the R-BT cluster of Betaproteobacteria and the AcI lineage of Actinobacteria (as % hybridized cells) taking up ATP, glucose-6-phosphate and glycerol-3-phosphate at the three concentrations added (0.2, 1, 5 nM) in the epilimnion (open bars) and hypolimnion (filled bars) of GKS (A, C, E) and PIB (B, D, F). Values are the mean of triplicate incubations ±1 SD. Asterisks indicate significant changes in active cells due to increasing substrate concentrations. Data points above the bars represent the mean bulk substrate uptake rates determined from duplicate incubations ±1 SD.
Mentions: The examined bacterial groups exhibited substrate-specific uptake patterns that were similar in both lakes (Fig. 1A and B). Betaproteobacteria and its R-BT cluster yielded the highest proportions of cells taking up Glu6P and Gly3P in the lakes, though more cells were labeled positive in GKS than in PIB. For both groups, the proportions of cells positive for ATP uptake represented ca. 20% of hybridized cells. Bacteroidetes and AcI Actinobacteria showed similar Glu6P and Gly3P uptake patterns (Fig. 1) and were often different from those of other bacterial groups (ANOVA, P < 0.01). In general, AcI Actinobacteria was weakly represented in the uptake of any substrate (range: ∼6–22% of hybridized cells) with the exception of Glu6P in PIB (range: ∼19–32% of hybridized cells; Figs 1B and 2F). By contrast, more Bacteroidetes cells were labeled positive for ATP uptake (22–36%) than for Gly3P or Glu6P uptake in the lakes. Around 30–55% of Alphaproteobacteria incorporated ATP and Gly3P (hypolimnion) in GKS and Glu6P in PIB.

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.