Bacterioplankton drawdown of coral mass-spawned organic matter

Ryan Guillemette, Ryo Kaneko, Jessica Blanton, Jasmine Tan, Matthias Witt, Samantha Hamilton, Eric E. Allen, Monica Medina, Koji Hamasaki, Boris P. Koch, Farooq Azam

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Coral reef ecosystems are highly sensitive to microbial activities that result from dissolved organic matter (DOM) enrichment of their surrounding seawater. However, the response to particulate organic matter (POM) enrichment is less studied. In a microcosm experiment, we tested the response of bacterioplankton to a pulse of POM from the mass-spawning of Orbicella franksi coral off the Caribbean coast of Panama. Particulate organic carbon (POC), a proxy measurement for POM, increased by 40-fold in seawater samples collected during spawning; 68% degraded within 66 h. The elevation of multiple hydrolases presumably solubilized the spawn-derived POM into DOM. A carbon budget constructed for the 275 µM of degraded POC showed negligible change to the concentration of dissolved organic carbon (DOC), indicating that the DOM was readily utilized. Fourier transform ion cyclotron resonance mass spectrometry shows that the DOM pool became enriched with heteroatom-containing molecules, a trend that suggests microbial alteration of organic matter. Our sensitivity analysis demonstrates that bacterial carbon demand could have accounted for a large proportion of the POC degradation. Further, using bromodeoxyuridine immunocapture in combination with 454 pyrosequencing of the 16S ribosomal RNA gene, we surmise that actively growing bacterial groups were the primary degraders. We conclude that coral gametes are highly labile to bacteria and that such large capacity for bacterial degradation and alteration of organic matter has implications for coral reef health and coastal marine biogeochemistry.

Original languageEnglish (US)
Pages (from-to)2238-2251
Number of pages14
JournalISME Journal
Volume12
Issue number9
DOIs
StatePublished - Sep 1 2018

Fingerprint

Anthozoa
drawdown
bacterioplankton
dissolved organic matter
particulate organic matter
corals
coral
soil organic matter
particulate organic carbon
Carbon
Particulate Matter
organic matter
Coral Reefs
coral reefs
coral reef
spawning
seawater
Seawater
degradation
biogeochemistry

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Guillemette, R., Kaneko, R., Blanton, J., Tan, J., Witt, M., Hamilton, S., ... Azam, F. (2018). Bacterioplankton drawdown of coral mass-spawned organic matter. ISME Journal, 12(9), 2238-2251. https://doi.org/10.1038/s41396-018-0197-7
Guillemette, Ryan ; Kaneko, Ryo ; Blanton, Jessica ; Tan, Jasmine ; Witt, Matthias ; Hamilton, Samantha ; Allen, Eric E. ; Medina, Monica ; Hamasaki, Koji ; Koch, Boris P. ; Azam, Farooq. / Bacterioplankton drawdown of coral mass-spawned organic matter. In: ISME Journal. 2018 ; Vol. 12, No. 9. pp. 2238-2251.
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abstract = "Coral reef ecosystems are highly sensitive to microbial activities that result from dissolved organic matter (DOM) enrichment of their surrounding seawater. However, the response to particulate organic matter (POM) enrichment is less studied. In a microcosm experiment, we tested the response of bacterioplankton to a pulse of POM from the mass-spawning of Orbicella franksi coral off the Caribbean coast of Panama. Particulate organic carbon (POC), a proxy measurement for POM, increased by 40-fold in seawater samples collected during spawning; 68{\%} degraded within 66 h. The elevation of multiple hydrolases presumably solubilized the spawn-derived POM into DOM. A carbon budget constructed for the 275 µM of degraded POC showed negligible change to the concentration of dissolved organic carbon (DOC), indicating that the DOM was readily utilized. Fourier transform ion cyclotron resonance mass spectrometry shows that the DOM pool became enriched with heteroatom-containing molecules, a trend that suggests microbial alteration of organic matter. Our sensitivity analysis demonstrates that bacterial carbon demand could have accounted for a large proportion of the POC degradation. Further, using bromodeoxyuridine immunocapture in combination with 454 pyrosequencing of the 16S ribosomal RNA gene, we surmise that actively growing bacterial groups were the primary degraders. We conclude that coral gametes are highly labile to bacteria and that such large capacity for bacterial degradation and alteration of organic matter has implications for coral reef health and coastal marine biogeochemistry.",
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Guillemette, R, Kaneko, R, Blanton, J, Tan, J, Witt, M, Hamilton, S, Allen, EE, Medina, M, Hamasaki, K, Koch, BP & Azam, F 2018, 'Bacterioplankton drawdown of coral mass-spawned organic matter', ISME Journal, vol. 12, no. 9, pp. 2238-2251. https://doi.org/10.1038/s41396-018-0197-7

Bacterioplankton drawdown of coral mass-spawned organic matter. / Guillemette, Ryan; Kaneko, Ryo; Blanton, Jessica; Tan, Jasmine; Witt, Matthias; Hamilton, Samantha; Allen, Eric E.; Medina, Monica; Hamasaki, Koji; Koch, Boris P.; Azam, Farooq.

In: ISME Journal, Vol. 12, No. 9, 01.09.2018, p. 2238-2251.

Research output: Contribution to journalArticle

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AU - Guillemette, Ryan

AU - Kaneko, Ryo

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AU - Koch, Boris P.

AU - Azam, Farooq

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Guillemette R, Kaneko R, Blanton J, Tan J, Witt M, Hamilton S et al. Bacterioplankton drawdown of coral mass-spawned organic matter. ISME Journal. 2018 Sep 1;12(9):2238-2251. https://doi.org/10.1038/s41396-018-0197-7