Microphytobenthic extracellular polymeric substances (EPS) in intertidal sediments fuel both generalist and specialist EPS‐degrading bacteria

Abstract

Microphytobenthic biofilms contain high concentrations of carbohydrate-rich extracellular polymeric substances (EPS) that are important in sediment carbon cycling. Field measurements at two locations in the Colne Estuary, U.K., showed that a significant curvilinear relationship explained 50% of the variability in chlorophyll a and EPS content. Estimates of EPS production, based on field data and published rates of production by diatoms, revealed that EPS turnover of 52% to 369% over the tidal cycle was required to account for field standing stocks. We investigated EPS degradation in sediment slurries using purified 13 C-EPS produced by the diatom Nitzschia tubicola. Although EPS constituted only 5% of the sediment dissolved organic carbon (DOC) pool, 100% of the added EPS was utilized within 30 h, before decreases in other sediment-carbohydrate fractions and DOC concentrations. A general 13 C enrichment of phospholipid fatty acids (PLFAs), representative of Gram-positive and Gram-negative bacteria, occurred within 6 h, with the PLFAs a15:0, i15:0, and 18:1v7c being highly enriched. The diatom PLFA 20:5v3 had relatively low but significant 13 C enrichment. Stable isotope probing of 16S ribosomal ribonucleic acid (RNA-SIP) at 30 h revealed 13 C-enriched sequences from the diatom genus Navicula; further evidence that diatoms assimilated the EPS, or EPS-breakdown products, from other diatom taxa. RNA-SIP also demonstrated a diverse range of highly 13 C-enriched bacterial taxa, including a distinct subset (Alphaproteobacteria and Gammaproteobacteria) found only in the heavily labeled microbial assemblages. Thus, cycling of diatom EPS is rapid, and involves a wide range of microbial taxa, including some apparent specialists.

Shifts in microbial community structure and function in light‐ and dark‐grown biofilms driven by warming

“…Common photosynthetic exudates include amino acids, organic acids, sugars and sugar‐alcohols (Watanabe et al ., ; Stengel et al ., ). Recently, Taylor and colleagues () demonstrated the utilization of algal produced extracellular polymeric substances by bacteria (especially Alphaproteobacteria and Gammaproteobacteria ) in marine microphytobenthic biofilms. Also, the significant increase in the leucine‐aminopeptidase in biofilms at L‐HT may indicate a greater decomposition of proteinaceous compounds excreted by primary producers (Ylla et al ., ; Díaz‐Villanueva et al ., ), as well as a decrease in the decomposition of polysaccharides.…”

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

“…The even labeling between different bacterial groups may be explained by a combination of diatom primary production dominating heterotrophic carbon cycling in this sediment and a wide variety of exudates produced by diatoms (although our results indicate that glucose in water-extractable EPS was a major intermediate). Taylor et al (2013) reported high label incorporation by diatoms, Alpha, and Gammaproteobacteria from isolated water-extractable EPS with RNA-SIP, but also showed the even labeling of general bacterial PLFA with PLFA-SIP. Miyatake et al (2013) also reported the even utilization of glucose (and other organic substrates) by most major groups in the microbial community of the sediment surface layer (0-2 cm).…”

“…In addition, we also measured 13 C labeling in bulk, water-extractable, and EDTA-extractable carbohydrates as well as SCOA in pore water using recently developed LC-IRMS methods to determine which intermediates were important in the transfer of organic matter from diatoms to heterotrophic bacteria. Although the relationship between diatom carbohydrates exudates and the heterotrophic bacterial community have been studied in intertidal sediments (Hanlon et al 2006;Haynes et al 2007;Bellinger et al 2009;Oakes et al 2012;Taylor et al 2013), we included SCOA as important intermediates in the anaerobic degradation of diatom material . The results were used to construct a conceptual model of the transfer of carbon in the diatom mat (Fig.…”

Use of glucose biosensors to measure extracellular glucose exudation by intertidal microphytobenthos in southern Tasmania

“…, Rivkin and Putt , Tuchman , Taylor et al. ) and may, in fact, be the norm rather than the exception (Mitra et al. , Selosse et al.…”