Different Types of Diatom-Derived Extracellular Polymeric Substances Drive Changes in Heterotrophic Bacterial Communities from Intertidal Sediments.

Julio Bohórquez,Sokratis Papaspyrou,Terry J Mcgenity,Alfonso Corzo,Graham J C Underwood,Emilio García-Robledo

doi:10.3389/fmicb.2017.00245

Abstract

Intertidal areas support extensive diatom-rich biofilms. Such microphytobenthic (MPB) diatoms exude large quantities of extracellular polymeric substances (EPS) comprising polysaccharides, glycoproteins and other biopolymers, which represent a substantial carbon pool. However, degradation rates of different EPS components, and how they shape heterotrophic communities in sediments, are not well understood. An aerobic mudflat-sediment slurry experiment was performed in the dark with two different EPS carbon sources from a diatom-dominated biofilm: colloidal EPS (cEPS) and the more complex hot-bicarbonate-extracted EPS. Degradation rate constants determined over 9 days for three sediment fractions [dissolved organic carbon (DOC), total carbohydrates (TCHO), and (cEPS)] were generally higher in the colloidal-EPS slurries (0.105–0.123 d−1) compared with the hot-bicarbonate-extracted-EPS slurries (0.060–0.096 d−1). Addition of hot-bicarbonate-EPS resulted in large increases in dissolved nitrogen and phosphorous by the end of the experiment, indicating that the more complex EPS is an important source of regenerated inorganic nutrients. Microbial biomass increased ~4–6-fold over 9 days, and pyrosequencing of bacterial 16S rRNA genes revealed that the addition of both types of EPS greatly altered the bacterial community composition (from 0 to 9 days) compared to a control with no added EPS. Bacteroidetes (especially Tenacibaculum) and Verrucomicrobia increased significantly in relative abundance in both the hot-bicarbonate-EPS and colloidal-EPS treatments. These differential effects of EPS fractions on carbon-loss rates, nutrient regeneration and microbial community assembly improve our understanding of coastal-sediment carbon cycling and demonstrate the importance of diverse microbiota in processing this abundant pool of organic carbon.

Highlights

Microphytobenthic communities inhabiting intertidal sediments, such as salt marshes and mudflats, exhibit high rates of primary production (Underwood et al, 2005) and are able to influence carbon and nitrogen fluxes in shallow-water systems (Perkins et al, 2001; Thornton et al, 2002; McKew et al, 2013)
The addition of extracellular polymeric substances (EPS) resulted in significantly higher Dissolved Organic Carbon (DOC) concentrations (between 3,600 and 3,800 μmol C L−1 on day 0, corresponding to 1.44 and 1.52 mmol C g−1 Wet Weight (WW) sediment, respectively) in all four EPS-addition treatments compared with the NoAdd-EPS control (DOC concentration 608 ± 74 μmol C L−1 or 0.24 mmol C g−1 WW sediment on day 0) (Figure 1A; Student-Newman-Keuls (SNK test), p < 0.05)
Values of k for DOC and colloidal EPS (cEPS) fractions in the +EPScoll treatment were significantly higher than those calculated for +EPSHB treatment

Summary

Introduction

Microphytobenthic communities inhabiting intertidal sediments, such as salt marshes and mudflats, exhibit high rates of primary production (Underwood et al, 2005) and are able to influence carbon and nitrogen fluxes in shallow-water systems (Perkins et al, 2001; Thornton et al, 2002; McKew et al, 2013). Colloidal EPS (EPScoll), water-soluble polymeric material isolated from colloidal aqueous extracts, and hot-bicarbonate extracted EPS (EPSHB), higher molecular weight (HMW) and more insoluble compounds such as tightly bound and capsular EPS, solubilized using hot bicarbonate extraction protocols (Bellinger et al, 2005; Aslam et al, 2016). These labile and bound EPS fractions differ in biochemical composition, and in the seasonal changes of their chemical composition (Pierre et al, 2014; Passarelli et al, 2015)

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Conclusion