A substantial fraction of phytoplankton-derived DON is resistant to degradation by a metabolically versatile, widely distributed marine bacterium

PLoS One. 2017 Feb 3;12(2):e0171391. doi: 10.1371/journal.pone.0171391. eCollection 2017.

Abstract

The capacity of bacteria for degrading dissolved organic nitrogen (DON) and remineralising ammonium is of importance for marine ecosystems, as nitrogen availability frequently limits productivity. Here, we assess the capacity of a widely distributed and metabolically versatile marine bacterium to degrade phytoplankton-derived dissolved organic carbon (DOC) and nitrogen. To achieve this, we lysed exponentially growing diatoms and used the derived dissolved organic matter (DOM) to support an axenic culture of Alteromonas sp.. Bacterial biomass (as particulate carbon and nitrogen) was monitored for 70 days while growth dynamics (cell count), DOM (DOC, DON) and dissolved nutrient concentrations were monitored for up to 208 days. Bacterial biomass increased rapidly within the first 7 days prior to a period of growth/death cycles potentially linked to rapid nutrient recycling. We found that ≈75% of the initial DOC and ≈35% of the initial DON were consumed by bacteria within 40 and 4 days respectively, leaving a significant fraction of DOM resilient to degradation by this bacterial species. The different rates and extents to which DOC and DON were accessed resulted in changes in DOM stoichiometry and the iterative relationship between DOM quality and bacterial growth over time influenced bacterial cell C:N molar ratio. C:N values increased to 10 during the growth phase before decreasing to values of ≈5, indicating a change from relative N-limitation/C-sufficiency to relative C-limitation/N-sufficiency. Consequently, despite its reported metabolic versatility, we demonstrate that Alteromonas sp. was unable to access all phytoplankton derived DOM and that a bacterial community is likely to be required. By making the relatively simple assumption that an experimentally derived fraction of DOM remains resilient to bacterial degradation, these experimental results were corroborated by numerical simulations using a previously published model describing the interaction between DOM and bacteria in marine systems, thus supporting our hypothesis.

MeSH terms

  • Bacteria / metabolism*
  • Biomass
  • Carbon / metabolism
  • Nitrogen / metabolism
  • Phytoplankton / metabolism*

Substances

  • Carbon
  • Nitrogen

Grants and funding

LP, DC and SK were part funded through the UK NERC (www.nerc.ac.uk/) national capability in sustained observation and marine modelling. LP was part funded through the NERC/Defra Shelf Seas Biogeochemistry program (NERC project number NE/K001876/1). We gratefully acknowledge support from the NERC (2014 Capital Investment award number CC059) for an Ultra High Performance Liquid Chromatograph-Time of Flight-Mass Spectrometer (uHPLC-TOF-MS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.