Resolving the paradox: Continuous cell-free alkaline phosphatase activity despite high phosphate concentrations

Thomson, Blair; Wenley, Jess; Currie, Kim; Hepburn, Christopher D.; Herndl, Gerhard J.; Baltar, Federico

doi:10.1016/j.marchem.2019.103671

Cited by 20 publications

(18 citation statements)

References 51 publications

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“…MEA ranged between 2.75-12.23 nmol L −1 h −1 (mean ± SE: 8.6 ± 1.5 nmol L −1 h −1 ), and DEA between 1.43-20.44 nmol L −1 h −1 (10.9 ± 4.7 nmol L −1 h −1 ). The MEA rates measured in the subantarctic waters were similar to the MEA rates measured previously in this water mass (Thomson et al, 2019) and in the North Atlantic by Steen et al (2016) but were frequently lower than some reports from the Mediterranean (Celussi and Del Negro, 2012;Celussi et al, 2019). In addition, our MEA rates were higher than those reported from the North Atlantic by (Baltar et al, 2009;Baltar et al, 2010;Baltar et al, 2013), North Pacific FIGURE 1 | Seasonal variability in temperature, phosphate, and nitrate (A), and chlorophyll-a and mean (±SE) bacterial abundance (B) in the epi-and mesopelagic layer at the study site in subantarctic waters.…”

Section: Resultssupporting

confidence: 86%

“…A large contribution of the cell-free EEA to the total EEA has important ecological and biogeochemical implications because cell-free enzymes can be temporally and/ or spatially decoupled from the producing cell (Baltar et al, 2010;Arnosti, 2011;Baltar et al, 2016b). Since residence times for cellfree enzymes are on the scale of days to weeks (Li et al, 1998;Ziervogel et al, 2010;Arnosti, 2011;Steen and Arnosti, 2011;Baltar et al, 2013;Thomson et al, 2019), the history of the water mass may have more explanatory power than the in situ microbial community in understanding EEA dynamics (Kamer and Rassoulzadegan, 1995;Baltar et al, 2010;Arnosti 2011;Baltar et al, 2016b). It has been suggested that a high proportion of cellfree MEA might explain the paradox of "high alkaline phosphatase activity at high P i concentration" (Thomson et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Since residence times for cellfree enzymes are on the scale of days to weeks (Li et al, 1998;Ziervogel et al, 2010;Arnosti, 2011;Steen and Arnosti, 2011;Baltar et al, 2013;Thomson et al, 2019), the history of the water mass may have more explanatory power than the in situ microbial community in understanding EEA dynamics (Kamer and Rassoulzadegan, 1995;Baltar et al, 2010;Arnosti 2011;Baltar et al, 2016b). It has been suggested that a high proportion of cellfree MEA might explain the paradox of "high alkaline phosphatase activity at high P i concentration" (Thomson et al, 2019). Thus, to understand the role of a particular type of EEA it is important to determine the contribution of the cell-free to the total EEA, and how it changes in response to different environmental conditions.…”

Section: Introductionmentioning

confidence: 99%

“…The contribution of cell-free to total DEA ranged from 13-49% in the only study where the cell-free fraction of DEA was studied (Sato et al, 2013). The percentage of cell-free to total MEA ranges from 12-100% throughout the water column (Hoppe, 1986;Li et al, 1998;Van Wambeke et al, 2002;Van Wambeke et al, 2009;Duhamel et al, 2011;Allison et al, 2012;Baltar et al, 2016b;Baltar et al, 2019;Thomson et al, 2019). The proportion of cell-free MEA (as well as of glucosidases and leucine aminopeptidase) tends to increase with depth from the epi-to bathypelagic waters (Baltar et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Relative Importance of Phosphodiesterase vs. Phosphomonoesterase (Alkaline Phosphatase) Activities for Dissolved Organic Phosphorus Hydrolysis in Epi- and Mesopelagic Waters

Thomson¹,

Wenley²,

Lockwood³

et al. 2020

Front. Earth Sci.

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Marine microbes use extracellular phosphatases to hydrolyze phosphate from organic matter. Dissolved organic phosphorus (DOP) is typically present in higher concentrations than phosphate in oceanic surface waters. Yet, the fate and role of different DOP components, such as phosphomonoester and phosphodiester, are poorly understood. Most of the investigations on extracellular enzymatic hydrolysis of marine DOP have focused on phosphomonoesterase (MEA) activity (i.e., alkaline phosphatase), whereas phosphodiesterase (DEA) measurements are scarce. This limits our understanding of the ecological and biogeochemical role of DOP sources other than P-monoesters in the sea. We determined extracellular MEA and DEA activities including their cell-free fractions on a bimonthly basis over 14 months in surface and mesopelagic subantarctic waters, thus covering a wide range of phosphate availability levels (from <0.5 to 2.3 µM). We found that DEA and MEA exhibit similar hydrolysis rates in surface as well as in mesopelagic waters. The MEA:DEA ratio varied between 0.38 and 5.42 during the study period, indicating potential differences in function and/or expression among the two enzyme groups, potentially reflecting differences in the availability and/or utilization of P-monoester and P-diester pools. Interestingly, the MEA:DEA was negatively correlated to phosphate (r −0.82, p 0.02, R 2 0.67) and positively with the inorganic N:P ratio (r 0.84, p 0.02, R 2 0.67), suggesting that the relative importance of DEA vs. MEA is linked to inorganic P availability and the N:P ratio. DEA was also related to the N:P ratio, both at the surface and at depth, suggesting DEA alone is sensitive to changes in the N:P ratio. The majority (>70%) of extracellular MEA and DEA was found in the cell-free fraction, increasing with depth for MEA. Our results indicated that DOP hydrolysis mediated by DEA in the surface as well as in dark ocean is as important as the frequently measured MEA.

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Section: Resultssupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Relative Importance of Phosphodiesterase vs. Phosphomonoesterase (Alkaline Phosphatase) Activities for Dissolved Organic Phosphorus Hydrolysis in Epi- and Mesopelagic Waters

Thomson¹,

Wenley²,

Lockwood³

et al. 2020

Front. Earth Sci.

Self Cite

View full text Add to dashboard Cite

show abstract

“…In many cases, Pase activity generally acts as a good indicator of the phosphorus supply for bacteria and phytoplankton (Hoppe, 2003; Luo et al, 2017). However, in some cases, Pase activities are decoupled from phosphate concentrations (Thomson et al, 2019). In comparison with the other enzymes tested in this study, Pase showed the highest activity at both 35 and 25°C (Figure 2E and Supplementary Figure S2E), the distributions of which were positively correlated with these of PO 4 3– (Pearson’s correlation test, for total EEA at 35°C, r = 0.86, p < 0.01; for dissolved EEA at 35°C, r = 0.41, p < 0.05; for total EEA at 25°C, r = 0.54, p < 0.05; for dissolved EEA at 25°C, r = 0.65, p < 0.05) (Figure 6).…”

Section: Discussionmentioning

confidence: 99%

Extracellular Enzyme Activity and Its Implications for Organic Matter Cycling in Northern Chinese Marginal Seas

Sun

et al. 2019

Front. Microbiol.

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Extracellular enzymes, initiating the degradation of organic macromolecules, are important functional components of marine ecosystems. Measuring in situ seawater extracellular enzyme activity (EEA) can provide fundamental information for understanding the biogeochemical cycling of organic matter in the ocean. Here we investigate the patterns of EEA and the major factors affecting the seawater EEA of Chinese marginal seas. The geographic distribution of EEA along a latitudinal transect was examined and found to be associated with dissolved organic carbon. Compared with offshore waters, inshore waters had higher enzyme activity. All the tested substrates were hydrolyzed at different rates and phosphatase, β-glucosidase and protease contributed greatly to summed hydrolysis rates. For any particular enzyme activity, the contribution of dissolved to total EEA was strongly heterogenous between stations. Comparisons of hydrolysis rates of the polymers and their corresponding oligomers suggest that molecule size does not necessarily limit the turnover of marine organic matter. In addition, several typical enzyme-producing clades, such as Bacteroidetes, Planctomycetes, Chloroflexi, Roseobacter, Alteromonas, and Pseudoalteromonas, were detected in the in situ environments. These enzyme-producing clades may be responsible for the production of different enzymes. Overall, each enzyme was found to flexibly respond to environmental conditions and were linked to microbial community composition. It is likely that this activity will profoundly affect organic matter cycling in the Chinese marginal seas.

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A sensitive fluorescent assay for measuring carbon‐phosphorus lyase activity in aquatic systems

Granzow

Sosa

Gonnelli

et al. 2021

Limnology & Ocean Methods

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In the oligotrophic ocean where inorganic phosphate (P i ) concentrations are low, microorganisms supplement their nutrient requirements with phosphorus (P) extracted from dissolved organic matter (DOM). Most P in DOM is bound as phosphate esters, which are hydrolyzed by phosphoesterases to P i . However, a large fraction of DOM-P occurs as phosphonates, reduced organophosphorus compounds with a C P bond that do not yield P i through simple ester hydrolysis alone. Phosphonates require an additional step that cleaves the C P bond and oxidizes P(III) to P(V) to yield P i . Most phosphonates are metabolized by the C-P lyase pathway, which cleaves C P bonds and oxidizes phosphonates to P i , enabling microbial assimilation. While the activity of common phosphoesterases such as alkaline phosphatase and phosphodiesterase can be measured by a fluorescent assay, a comparable method to assess C-P lyase activity (CLA) in natural water samples does not exist. To address this, we synthesized a dansyl-labeled phosphonate compound, and measured its hydrolysis by C-P lyase using high performance liquid chromatography. We found that laboratory cultures of marine bacteria expressing the C-P lyase pathway are able to hydrolyze the dansyl phosphonate, while bacteria expressing other phosphonate degradation pathways do not. Finally, we performed several field tests of the assay to measure water column profiles of CLA at Sta. ALOHA in the North Pacific Subtropical Gyre. Activity was elevated near the deep chlorophyll maximum suggesting high levels of phosphonate degradation in that region.

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Resolving the paradox: Continuous cell-free alkaline phosphatase activity despite high phosphate concentrations

Cited by 20 publications

References 51 publications

Relative Importance of Phosphodiesterase vs. Phosphomonoesterase (Alkaline Phosphatase) Activities for Dissolved Organic Phosphorus Hydrolysis in Epi- and Mesopelagic Waters

Relative Importance of Phosphodiesterase vs. Phosphomonoesterase (Alkaline Phosphatase) Activities for Dissolved Organic Phosphorus Hydrolysis in Epi- and Mesopelagic Waters

Extracellular Enzyme Activity and Its Implications for Organic Matter Cycling in Northern Chinese Marginal Seas

A sensitive fluorescent assay for measuring carbon‐phosphorus lyase activity in aquatic systems

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