Tracing carbon and nitrogen incorporation and pathways in the microbial community of a photic subtidal sand

Abstract

The pathways and fate of C and N in the microbial compartment of a coastal permeable sandy sediment in the photic zone were studied in a pulse-chase experiment.13 C-bicarbonate and 15 N-nitrate were added to the water column on top of 5 sediment cores incubated in 4 transparent and 1 opaque laboratory chambers. After 9 h of labelling in the light and dark, stable isotope incorporation by microphytobenthos (MPB) and bacteria was quantified over a period of 4 d through the analysis of phospholipid-derived fatty acids (PLFA) and hydrolysable amino acids (HAA). 13 C was fixed by MPB, and more than 50% was directed to the production of extracellular polymeric substance (EPS). MPB 15 N incorporation was similar in the dark and in the light. Bacterial activity appeared to have 2 effects that depended on sediment depth: at the sediment surface, there was a steady increase of label in the bacterial PLFA, suggesting metabolism of label-containing EPS; in the subsurface layers, uniform enrichment started immediately after the labelling procedure, indicating continuous incorporation of inorganic C by chemoautotrophic bacteria (Cbac). This experiment demonstrates the efficient transfer of inorganic C and N to the benthic community through the activities of photo-and chemoautotrophic microorganisms, and the role of EPS as a carrier of energy to the benthic microbial food web.KEY WORDS: Microphytobenthos · Cyanobacteria · EPS · PLFA · Biomarkers · Amino acids · Chemoautotrophy · Permeable sediment · 15 N · 13 C · Stable isotopes · Nitrate Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 53: [257][258][259][260][261][262][263][264][265][266][267][268][269] 2008 ( Fig. 1). In the surface layer, MPB often represents the most important component in terms of biomass and turnover and modulates C and N transfer across the sediment -water interface (MacIntyre et al. 1996, Sundback et al. 1996. Although C fixation and N assimilation are often closely related to the buildup of biomass, a large part of the C fixed may be diverted to synthesis of extracellular polymeric substances (EPS) that can account for a large fraction of organic C present in the sediment (Smith & Underwood 1998, Goto et al. 1999, Wieland et al. 2008. The second major pathway is heterotrophy: the utilisation of detritus, MPB, EPS and other organic substrates by heterotrophic bacteria (Hbac), meiofauna and macrofauna. Heterotrophic benthic organisms produce new biomass (secondary production) and govern mineralization of organic matter. The third metabolic pathway is chemoautotrophy: the fixation of CO 2 using the energy released upon oxidation of reduced inorganic compounds. This topic has received limited attention in the literature, yet it may constitute a significant pathway close to redox boundaries (Kristensen & Hansen 1995, Thomsen & Kristensen 1997.Although the biological importance of subtidal permeable sediments was recognized decades ago (Riedl et al. 1972), these systems remain poorly documented. ...

Fate of macroalgae in benthic systems: carbon and nitrogen cycling within the microbial community

“…BMA have also been shown to take up dissolved organic N directly (Nilsson & Sundback 1996). To complete the cycle, bacteria then recycled labeled BMA detritus and/or extrapolymeric substances exuded by the BMA (Smith & Underwood 1998, Veuger et al 2007a, Evrard et al 2008. Good agreement between bacterial and BMA fatty acids supports a tight coupling between these communities (r 2 = 0.93 and 0.92 for HIB and IWB, respectively), although bacteria have also been shown to recycle nutrients independent of BMA by reincorporating their own degradation products (Veuger et al 2006(Veuger et al , 2007a.…”

Macrofauna regulate heterotrophic bacterial carbon and nitrogen incorporation in low-oxygen sediments

“…To date, application of this technique in OMZ-impacted sediments has focused upon the fate of organic carbon, within shipboard incubations (for example, Woulds et al, 2007;Andersson et al, 2008;Moodley et al, 2011). The advent of a method to trace 15 N incorporation into hydrolysable amino acids (HAAs), including the bacteria-specific amino-acid D-alanine, (Veuger et al, , 2007b makes it possible to empirically assess bacterial N utilisation and de-coupling of C and N in marine sediments (Cook et al, 2007;Veuger and Middelburg, 2007;Evrard et al, 2008).…”

Tracing carbon flow from microphytobenthos to major bacterial groups in an intertidal marine sediment by using an in situ 13C pulse‐chase method

“…However, there are only a limited number of studies that link in situ carbon flow from diatoms directly to heterotrophic microbes and also identify in detail the responsible microorganisms . Middelburg et al (2000) and Evrard et al (2008) have reported rapid transfer of carbon from microphytobenthos to bacterial biomass by combining in situ 13 C pulse-chase labeling and phospholipid-derived fatty acid (PLFA) biomarker analysis in order to differentiate between labeling in algae and heterotrophic bacteria. Previous studies suggested that EPS-derived carbohydrates were major intermediates in the transfer of organic matter between benthic diatoms and heterotrophic bacteria (Bellinger et al 2009;Oakes et al 2010;Taylor et al 2013).…”