Evidence for key enzymatic controls on metabolism of Arctic river organic matter

Paul J. Mann, William V. Sobczak, Madeleine M. Larue, Ekaterina Bulygina, Anna Davydova, Jorien E. Vonk, John Schade, Sergei Davydov, Nikita Zimov, Robert M. Holmes, Robert G M Spencer

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Permafrost thaw in the Arctic driven by climate change is mobilizing ancient terrigenous organic carbon (OC) into fluvial networks. Understanding the controls on metabolism of this OC is imperative for assessing its role with respect to climate feedbacks. In this study, we examined the effect of inorganic nutrient supply and dissolved organic matter (DOM) composition on aquatic extracellular enzyme activities (EEAs) in waters draining the Kolyma River Basin (Siberia), including permafrost-derived OC. Reducing the phenolic content of the DOM pool resulted in dramatic increases in hydrolase EEAs (e.g., phosphatase activity increased >28-fold) supporting the idea that high concentrations of polyphenolic compounds in DOM (e.g., plant structural tissues) inhibit enzyme synthesis or activity, limiting OC degradation. EEAs were significantly more responsive to inorganic nutrient additions only after phenolic inhibition was experimentally removed. In controlled mixtures of modern OC and thawed permafrost endmember OC sources, respiration rates per unit dissolved OC were 1.3-1.6 times higher in waters containing ancient carbon, suggesting that permafrost-derived OC was more available for microbial mineralization. In addition, waters containing ancient permafrost-derived OC supported elevated phosphatase and glucosidase activities. Based on these combined results, we propose that both composition and nutrient availability regulate DOM metabolism in Arctic aquatic ecosystems. Our empirical findings are incorporated into a mechanistic conceptual model highlighting two key enzymatic processes in the mineralization of riverine OM: (i) the role of phenol oxidase activity in reducing inhibitory phenolic compounds and (ii) the role of phosphatase in mobilizing organic P. Permafrost-derived DOM degradation was less constrained by this initial 'phenolic-OM' inhibition; thus, informing reports of high biological availability of ancient, permafrost-derived DOM with clear ramifications for its metabolism in fluvial networks and feedbacks to climate.

Original languageEnglish
Pages (from-to)1089-1100
Number of pages12
JournalGlobal Change Biology
Volume20
Issue number4
DOIs
Publication statusPublished - Apr 2014

Fingerprint

Organic carbon
Rivers
Metabolism
Permafrost
Biological materials
permafrost
Carbon
metabolism
organic carbon
dissolved organic matter
organic matter
river
Enzyme activity
phosphatase
enzyme activity
Phosphoric Monoester Hydrolases
Nutrients
Enzymes
Climate
Water

Keywords

  • Aquatic
  • Arctic
  • Biogeochemistry
  • Dissolved organic matter
  • Enzymes
  • Global change
  • Organic matter decomposition
  • Permafrost

Cite this

Mann, P. J., Sobczak, W. V., Larue, M. M., Bulygina, E., Davydova, A., Vonk, J. E., ... Spencer, R. G. M. (2014). Evidence for key enzymatic controls on metabolism of Arctic river organic matter. Global Change Biology, 20(4), 1089-1100. https://doi.org/10.1111/gcb.12416
Mann, Paul J. ; Sobczak, William V. ; Larue, Madeleine M. ; Bulygina, Ekaterina ; Davydova, Anna ; Vonk, Jorien E. ; Schade, John ; Davydov, Sergei ; Zimov, Nikita ; Holmes, Robert M. ; Spencer, Robert G M. / Evidence for key enzymatic controls on metabolism of Arctic river organic matter. In: Global Change Biology. 2014 ; Vol. 20, No. 4. pp. 1089-1100.
@article{20b721b1daf94df28bc653e6c3a02589,
title = "Evidence for key enzymatic controls on metabolism of Arctic river organic matter",
abstract = "Permafrost thaw in the Arctic driven by climate change is mobilizing ancient terrigenous organic carbon (OC) into fluvial networks. Understanding the controls on metabolism of this OC is imperative for assessing its role with respect to climate feedbacks. In this study, we examined the effect of inorganic nutrient supply and dissolved organic matter (DOM) composition on aquatic extracellular enzyme activities (EEAs) in waters draining the Kolyma River Basin (Siberia), including permafrost-derived OC. Reducing the phenolic content of the DOM pool resulted in dramatic increases in hydrolase EEAs (e.g., phosphatase activity increased >28-fold) supporting the idea that high concentrations of polyphenolic compounds in DOM (e.g., plant structural tissues) inhibit enzyme synthesis or activity, limiting OC degradation. EEAs were significantly more responsive to inorganic nutrient additions only after phenolic inhibition was experimentally removed. In controlled mixtures of modern OC and thawed permafrost endmember OC sources, respiration rates per unit dissolved OC were 1.3-1.6 times higher in waters containing ancient carbon, suggesting that permafrost-derived OC was more available for microbial mineralization. In addition, waters containing ancient permafrost-derived OC supported elevated phosphatase and glucosidase activities. Based on these combined results, we propose that both composition and nutrient availability regulate DOM metabolism in Arctic aquatic ecosystems. Our empirical findings are incorporated into a mechanistic conceptual model highlighting two key enzymatic processes in the mineralization of riverine OM: (i) the role of phenol oxidase activity in reducing inhibitory phenolic compounds and (ii) the role of phosphatase in mobilizing organic P. Permafrost-derived DOM degradation was less constrained by this initial 'phenolic-OM' inhibition; thus, informing reports of high biological availability of ancient, permafrost-derived DOM with clear ramifications for its metabolism in fluvial networks and feedbacks to climate.",
keywords = "Aquatic, Arctic, Biogeochemistry, Dissolved organic matter, Enzymes, Global change, Organic matter decomposition, Permafrost",
author = "Mann, {Paul J.} and Sobczak, {William V.} and Larue, {Madeleine M.} and Ekaterina Bulygina and Anna Davydova and Vonk, {Jorien E.} and John Schade and Sergei Davydov and Nikita Zimov and Holmes, {Robert M.} and Spencer, {Robert G M}",
year = "2014",
month = "4",
doi = "10.1111/gcb.12416",
language = "English",
volume = "20",
pages = "1089--1100",
journal = "Global Change Biology",
issn = "1354-1013",
publisher = "Wiley-Blackwell Publishing",
number = "4",

}

Mann, PJ, Sobczak, WV, Larue, MM, Bulygina, E, Davydova, A, Vonk, JE, Schade, J, Davydov, S, Zimov, N, Holmes, RM & Spencer, RGM 2014, 'Evidence for key enzymatic controls on metabolism of Arctic river organic matter' Global Change Biology, vol. 20, no. 4, pp. 1089-1100. https://doi.org/10.1111/gcb.12416

Evidence for key enzymatic controls on metabolism of Arctic river organic matter. / Mann, Paul J.; Sobczak, William V.; Larue, Madeleine M.; Bulygina, Ekaterina; Davydova, Anna; Vonk, Jorien E.; Schade, John; Davydov, Sergei; Zimov, Nikita; Holmes, Robert M.; Spencer, Robert G M.

In: Global Change Biology, Vol. 20, No. 4, 04.2014, p. 1089-1100.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Evidence for key enzymatic controls on metabolism of Arctic river organic matter

AU - Mann, Paul J.

AU - Sobczak, William V.

AU - Larue, Madeleine M.

AU - Bulygina, Ekaterina

AU - Davydova, Anna

AU - Vonk, Jorien E.

AU - Schade, John

AU - Davydov, Sergei

AU - Zimov, Nikita

AU - Holmes, Robert M.

AU - Spencer, Robert G M

PY - 2014/4

Y1 - 2014/4

N2 - Permafrost thaw in the Arctic driven by climate change is mobilizing ancient terrigenous organic carbon (OC) into fluvial networks. Understanding the controls on metabolism of this OC is imperative for assessing its role with respect to climate feedbacks. In this study, we examined the effect of inorganic nutrient supply and dissolved organic matter (DOM) composition on aquatic extracellular enzyme activities (EEAs) in waters draining the Kolyma River Basin (Siberia), including permafrost-derived OC. Reducing the phenolic content of the DOM pool resulted in dramatic increases in hydrolase EEAs (e.g., phosphatase activity increased >28-fold) supporting the idea that high concentrations of polyphenolic compounds in DOM (e.g., plant structural tissues) inhibit enzyme synthesis or activity, limiting OC degradation. EEAs were significantly more responsive to inorganic nutrient additions only after phenolic inhibition was experimentally removed. In controlled mixtures of modern OC and thawed permafrost endmember OC sources, respiration rates per unit dissolved OC were 1.3-1.6 times higher in waters containing ancient carbon, suggesting that permafrost-derived OC was more available for microbial mineralization. In addition, waters containing ancient permafrost-derived OC supported elevated phosphatase and glucosidase activities. Based on these combined results, we propose that both composition and nutrient availability regulate DOM metabolism in Arctic aquatic ecosystems. Our empirical findings are incorporated into a mechanistic conceptual model highlighting two key enzymatic processes in the mineralization of riverine OM: (i) the role of phenol oxidase activity in reducing inhibitory phenolic compounds and (ii) the role of phosphatase in mobilizing organic P. Permafrost-derived DOM degradation was less constrained by this initial 'phenolic-OM' inhibition; thus, informing reports of high biological availability of ancient, permafrost-derived DOM with clear ramifications for its metabolism in fluvial networks and feedbacks to climate.

AB - Permafrost thaw in the Arctic driven by climate change is mobilizing ancient terrigenous organic carbon (OC) into fluvial networks. Understanding the controls on metabolism of this OC is imperative for assessing its role with respect to climate feedbacks. In this study, we examined the effect of inorganic nutrient supply and dissolved organic matter (DOM) composition on aquatic extracellular enzyme activities (EEAs) in waters draining the Kolyma River Basin (Siberia), including permafrost-derived OC. Reducing the phenolic content of the DOM pool resulted in dramatic increases in hydrolase EEAs (e.g., phosphatase activity increased >28-fold) supporting the idea that high concentrations of polyphenolic compounds in DOM (e.g., plant structural tissues) inhibit enzyme synthesis or activity, limiting OC degradation. EEAs were significantly more responsive to inorganic nutrient additions only after phenolic inhibition was experimentally removed. In controlled mixtures of modern OC and thawed permafrost endmember OC sources, respiration rates per unit dissolved OC were 1.3-1.6 times higher in waters containing ancient carbon, suggesting that permafrost-derived OC was more available for microbial mineralization. In addition, waters containing ancient permafrost-derived OC supported elevated phosphatase and glucosidase activities. Based on these combined results, we propose that both composition and nutrient availability regulate DOM metabolism in Arctic aquatic ecosystems. Our empirical findings are incorporated into a mechanistic conceptual model highlighting two key enzymatic processes in the mineralization of riverine OM: (i) the role of phenol oxidase activity in reducing inhibitory phenolic compounds and (ii) the role of phosphatase in mobilizing organic P. Permafrost-derived DOM degradation was less constrained by this initial 'phenolic-OM' inhibition; thus, informing reports of high biological availability of ancient, permafrost-derived DOM with clear ramifications for its metabolism in fluvial networks and feedbacks to climate.

KW - Aquatic

KW - Arctic

KW - Biogeochemistry

KW - Dissolved organic matter

KW - Enzymes

KW - Global change

KW - Organic matter decomposition

KW - Permafrost

UR - http://www.scopus.com/inward/record.url?scp=84896719054&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84896719054&partnerID=8YFLogxK

U2 - 10.1111/gcb.12416

DO - 10.1111/gcb.12416

M3 - Article

VL - 20

SP - 1089

EP - 1100

JO - Global Change Biology

JF - Global Change Biology

SN - 1354-1013

IS - 4

ER -