Dose-dependent regulation of microbial activity on sinking particles by polyunsaturated aldehydes: Implications for the carbon cycle

Abstract

Diatoms and other phytoplankton play a crucial role in the global carbon cycle, fixing CO 2 into organic carbon, which may then be exported to depth via sinking particles. The molecular diversity of this organic carbon is vast and many highly bioactive molecules have been identified. Polyunsaturated aldehydes (PUAs) are bioactive on various levels of the marine food web, and yet the potential for these molecules to affect the fate of organic carbon produced by diatoms remains an open question. In this study, the effects of PUAs on the natural microbial assemblages associated with sinking particles were investigated. Sinking particles were collected from 150 m in the water column and exposed to varying concentrations of PUAs in dark incubations over 24 h. PUA doses ranging from 1 to 10 μM stimulated respiration, organic matter hydrolysis, and cell growth by bacteria associated with sinking particles. PUA dosages near 100 μM appeared to be toxic, resulting in decreased bacterial cell abundance and metabolism, as well as pronounced shifts in bacterial community composition. Sinking particles were hot spots for PUA production that contained concentrations within the stimulatory micromolar range in contrast to previously reported picomolar concentrations of these compounds in bulk seawater. This suggests PUAs produced in situ stimulate the remineralization of phytoplankton-derived sinking organic matter, decreasing carbon export efficiency, and shoaling the average depths of nutrient regeneration. Our results are consistent with a "bioactivity hypothesis" for explaining variations in carbon export efficiency in the oceans. polyunsaturated aldehydes | sinking particles | particle-associated bacteria | marine carbon cycle | bioactivity hypothesis

Quorum Sensing Plays a Complex Role in Regulating the Enzyme Hydrolysis Activity of Microbes Associated with Sinking Particles in the Ocean

“…It is possible that the responses we observed over longer timescales (i.e., 12-and 24-h) were influenced by community shifts, although we have no data that speaks to this directly. Edwards et al (2015) recently showed that additions of diatom-derived polyunsaturated aldehydes led to similar changes in enzyme activity after 24 h of incubation, but did not affect major shifts in community structure except at very high concentrations.…”

“…of infochemicals on the activity of particle-associated bacterial assemblages, but they have thus far affirmed that bacterial signaling systems are involved in, and may either enhance or inhibit the rate of the degradation of sinking POC (Hmelo et al, 2011;Van Mooy et al, 2012;Edwards et al, 2015).…”

Linking biochemical properties of particles to particle‐attached and free‐living bacterial community structure along the particle density gradient from freshwater to open ocean

“…Thus, we hypothesize that particles have a stronger influence on particle‐attached than free‐living bacterial communities. However, very few studies have addressed the relationship between particle composition and microbes [ Edwards et al ., ]. The molecular characterization of particle‐attached microbiota and free‐living counterparts would help to reveal specific details about the mechanisms regulating fluxes of particulate organic carbon (POC) to DOC, which will ultimately influence the rates of carbon export and storage [ Jiao et al ., , ].…”

A fast and direct liquid chromatography‐mass spectrometry method to detect and quantify polyunsaturated aldehydes and polar oxylipins in diatoms

“…The sample preparation was modified according to former protocols (Wichard et al 2005b) to achieve a fast analytical workflow allowing cell enrichment, cell wounding, incubation for wound-activated PUA production, and removal of suspended cell material within 20 min before UHPLC-HRMS measurement. The novel analytical approach allows determining PUAs within the complex cell-free algal lysate matrix without work-and time-intensive derivatization procedures as introduced by d' Ippolito et al (2002a), Wichard et al (2005b), or Edwards et al (2015.…”

“…This has been proven as a very robust and reliable method used by several laboratories (Taylor et al 2007;Morillo-Garcia et al 2014;Lavrentyev et al 2015). Derivatization is followed by extraction using hexane giving highly reproducible results in GC-MS. Alternatively, high performance liquid chromatography (HPLC)-separation of PUA-derived dinitrophenylhydrazones has been introduced on liquid-liquid extracts of PUAs (Edwards et al 2015). Recent studies focusing on oxylipin profiles of diatoms not only analyzed the volatile oxylipins using GC-MS but also screened for nonvolatile oxylipins such as fatty acid hydroperoxides, hydroxy-, epoxyhydroxy fatty acids or x-oxo-acids using liquid chromatography-mass spectrometry (LC-MS) (Barreiro et al 2011;Ianora et al 2015).…”