We studied patterns of production and loss of four different extracellular polymeric substance (EPS) fractionscolloidal carbohydrates, colloidal EPS (cEPS), hot water (HW)-extracted and hot bicarbonate (HB)-extracted fractions-and community profiles of active (RNA) bacterial communities by use of Terminal-Restriction Fragment Length Polymorphism (T-RFLP) analysis of reverse transcription-polymerase chain reaction amplified 16S rRNA in mudflats in the Colne Estuary, United Kingdom, over two tidal emersion-immersion cycles. Colloidal carbohydrates and intracellular storage carbohydrate (HW) increased during tidal emersion and declined during tidal cover. The dynamics of cEPS and uronic acid content were closely coupled, as were the HB fraction and HB uronic acids. Changes in monosaccharide profiles of HW and HB fractions occurred during the diel period, with some similarity between cEPS and HB fractions. Increasing enzymatic release rates of reducing sugars and increased reducing sugar content were correlated with increased concentrations of colloidal carbohydrate and cEPS during the illuminated emersion period, and with the amount of HB-extracted uronic acids (the most refractory EPS fraction measured). Loss of reducing sugars was high, with sediment concentrations far below those predicted by the measured in situ release rates. T-RFLP analysis revealed no significant shifts in the overall taxonomic composition of the active bacterial community. However, 12 of the 59 terminal restriction fragments identified showed significant changes in relative abundance during the tidal cycle. Changes in the relative abundance of three particular terminal restriction fragments (bacterial taxa) were positively correlated to the rate of extracellular hydrolysis. Losses of chlorophyll a and colloidal and cEPS (up to 50-60%) occurred mainly in the first 30 min after tidal cover. About half of this may be owing to in situ degradation, with ''wash away'' into the water column accounting for the remainder.Microphytobenthic biofilms in intertidal sediments play an important role in the ecology of estuarine systems (Under-1 Corresponding author (gjcu@essex.ac.uk).
The importance of temporal changes in the vertical distribution of microphytobenthic algae on the overall functioning of intertidal biofilms were investigated with low-temperature scanning electron microscopy and high-resolution single-cell fluorescence imaging of photosystem II efficiency (estimated by the fluorescence parameter F / Ј q F ) in intact cores maintained in tidal mesocosms. Early morning biofilms consisted of smaller naviculoid and Ј m nitzschioid taxa or euglenoid species. By midday, Gyrosigma balticum and Pleurosigma angulatum were dominant. Some taxa (e.g., Plagiotropis vitrea) disappeared from surface layers after midday. Species composition continued to change toward the end of the photoperiod, with G. balticum dominating in diatom-rich biofilms. In Euglena-rich biofilms, initial dense surface films of euglenids became progressively dominated by smaller diatoms. F /F (mea-Ј Ј q m sured at a photosynthetically active photon flux density (PPFD) of 220 mol m Ϫ2 s Ϫ1) of individual cells of all taxa declined significantly after midday, but increased toward dusk. There were significant differences in F /F between Ј Ј q m species, particularly after midday. F /F versus irradiance curves and relative electron transport rate (rETR max ) Ј Ј q m showed higher efficiencies and rETR max for euglenids, whereas G. balticum, Nitzschia dubia, and small Nitzschia sp. were shade-adapted with low values of F /F m Ј, rETR max , and E sat . G. balticum, P. vitrea, and N. dubia showed Ј q rapid vertical migration away from the surface with increasing irradiance. Euglenids, P. angulatum, and N. dubia exhibited their highest rETR max values at midday. E sat for algal cells was between 500 and 600 mol m Ϫ2 s Ϫ1 , except for N. dubia and small Nitzschia sp., which had an E sat of 300 mol m Ϫ2 s Ϫ1. Differences in behavioral and photophysiological traits between microphytobenthic taxa could be a form of niche separation and need to be incorporated into conceptual models of daily patterns of production in intertidal biofilms.
Rates of primary production by intertidal microphytobenthos within biofilms have been shown to be very high. An essential step toward assessing the contribution of individual species to this level of production is the in vivo measurement of photosynthetic efficiency from individual cells. A strong relationship between photosystem II photochemical efficiency and the fluorescence parameter Fq'/Fm′ (where Fq′ = Fm′ − F′) has been established within higher plants and unicellular algae. Calculation of Fq′/Fm′ requires measurement under constant light (at the F′ level of fluorescence) and during a pulse of saturating light (at the Fm′ level of fluorescence). High‐resolution imaging of chlorophyll fluorescence at the F′ and Fm′ levels has allowed the construction of Fq′/Fm′ images from individual cells of several species of diatom and Euglena sp. within intact biofilms. No species differences in the values of Fq′/Fm′ were observed at low levels of incident light. However, Euglena sp. showed significantly higher Fq′/Fm′ values at moderate to high incident light levels than all of the diatom species. Endogenous rhythms of vertical migration during tidal exposure and peaks in photosystem II photochemical efficiency at low tide could also be followed using this technique. Clear differences were observed in the migration of individual taxa to the surface of the biofilm. Images of Fq′/Fm′ were also used to assess the scale of heterogeneity for this parameter. Overall, these data demonstrate that high‐resolution imaging of chlorophyll fluorescence is a valuable technique that allows for determination of the photosystem II photochemical efficiency from different microphytobenthic taxa within biofilms.
Microphytobenthic biofilms in estuarine sediments, consisting of photosynthetic microalgae, heterotrophic bacteria and their associated exopolymers, contain high concentrations of watersoluble colloidal carbohydrates that can be separated using ethanol precipitation into low molecular weight (LMW) carbohydrate and colloidal extracellular polymeric substances (cEPS). These carbohydrate-rich components are potentially a significant carbon source, but utilisation processes are not well described. Short-term (24 h) degradation studies using sediment slurries with enhanced colloidal carbohydrate and cEPS concentrations found rapid increases in LMW carbohydrate concentrations during the first 4 h, with subsequent utilisation of LMW carbohydrate and cEPS after 8 to 24 h. The cEPS contribution to the colloidal carbohydrate pool increased (16 to between 67 and 97%) in control and colloidal carbohydrate-enriched slurries, with decreasing glucose and increasing mannose and xylose contents within the EPS fraction after 24 h, suggesting initial utilisation of glucose-rich components in preference to more complex EPS. When cEPS concentrations were increased (cEPS-enrichment), there was greater EPS utilisation, and a decline in the relative contribution of EPS (72 to 31% of the colloidal carbohydrate fraction), without significant change in the monosaccharide composition in the cEPS fraction. Using selective media with cEPS as a sole carbon source, a β-proteobacterium Variovorax sp. Alr1 was isolated. Variovorax sp. Alr1 grew rapidly on cEPS as a sole carbon source, with increasing β-glucosidase activity and the production of new EPS rich in rhamnose, galactose and fucose, but showed only limited growth on EPS extracted from sediment using a hot-bicarbonate extraction procedure, despite increases in β-glucosidase and aminopeptidase activity. Differences in the short-term lability of different fractions of sediment carbohydrate and the ability of a heterotroph to utilise these fractions suggests a range of different heterotrophic bacteria may be involved in the complete degradation of EPS in situ. KEY WORDS: Biofilms · EPS · Microphytobenthos · Exopolymers · Degradation · Mudflats Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 379: [45][46][47][48][49][50][51][52][53][54][55][56][57][58] 2009 2003, Underwood & Paterson 2003). These microphytobenthic (MPB) biofilms are sites of high rates of biogeochemical cycling, exhibiting complex rhythms of photosynthetic activity (Pinckney & Zingmark 1991, mediating nitrogen cycling processes (Risgaard-Petersen 2003, Cook et al. 2007) and contributing to the physical stability of the underlying sediment (Orvain et al. 2003, Underwood & Paterson 2003.The production of EPS by intertidal biofilms dominated by pennate diatoms is well described. Pennate (bilaterally symmetrical) diatoms produce EPS that predominantly consist of polysaccharides (Hoagland et al. 1993, Underwood & Paterson 2003. The amount of photoassimilates excreted as...
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