Free-living and particle-associated prokaryote metabolism in giant kelp forests: Implications for carbon flux in a sub-Antarctic coastal area

Abstract

Extensive beds of large subtidal kelps are characteristic of many temperate and subpolar coastlines. They provide habitats for a wide range of other species and are sites of high primary production that generate large quantities of water-borne particles and dissolved organic compounds that support distinctive communities of prokaryotes. We measured prokaryotic metabolism along transects from the shore to the outside of three giant kelp forests (Macrocystis pyrifera) located in the shelf waters of the Prince Edward Islands (Southern Ocean). Abundance, heterotrophic production (PHP), respiration rates (R-ETS) and growth efficiencies (PGE) were investigated within the particle-associated (PA) and the free-living (FL) communities. Temperature, salinity and inorganic nutrient concentrations indicated distinct hydrological differences among the kelp forests that were related to different levels of freshwater input through island runoff. In contrast, detritus and particulate organic matter concentrations showed a common pattern, decreasing from the near-shore to offshore at all sampling sites, suggesting the retention of organically enriched water masses inshore of the kelp forests. While FL and PA abundances did not differ significantly along transects, FL and PA-PHP and PGE all varied significantly across the kelp forests, following the same pattern across each forest. PA-PGE was significantly higher than FL-PGE in the near-shore waters and farther offshore, while FL-PGE was higher or equal to PA-PGE inside the kelp. This shift can be interpreted in terms of gradients in both the age and origins of organic material across the kelp forests. Higher PA-PGE implies that a larger fraction of organic carbon on colonized particles is converted into prokaryotic biomass and so becomes available to higher trophic levels inshore and offshore of M. pyrifera forests than inside the kelp bed. In contrast, low PA-PGE suggests that a large quantity of carbon passes through the PAcommunity and is mainly respired within the kelp forest. These results suggest the retention of particles within giant kelp forests. In controlling the metabolic activity of PA and FL prokaryotes, this retention will influence overall carbon flux around the archipelago. In particular, the observation of a common pattern across different M. pyrifera forests has important implications for the role of this species as an autogenic ecological engineer in coastal environments.

Prokaryotic abundance, cell size and extracellular enzymatic activity in a human impacted and mangrove dominated tropical estuary (Can Gio, Vietnam)

“…In a tidal estuary exhibiting high loads of suspended matter, particle-attached prokaryotes can reach up to 80% of total abundance (De Souza et al 2003). It has previously been observed that particle-attached prokaryotes were more active than free-living cells (Grossart et al 2007a, 2007b, Schapira et al 2012. Although in our study no difference could be evidenced in prokaryote abundance between water layers, the proportion of J o u r n a l P r e -p r o o f particle-attached cells may have been higher in the bottom compared to other layers, due to higher loads of SPM (Fig.…”

Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem

“…Another possibility is the involvement of some of these Flavobacteria in the degradation of macroscopic algae, such as the Phaeophyta kelps (brown algae), which are members of the order Laminariales. Extensive beds of large subtidal kelps are typical of the temperate Pacific Northwest coastline, they generate large quantities of water-borne particles and dissolved organic compounds that support distinctive communities of prokaryotes (Schapira et al, 2012). Genomes of many Flavobacteria, including the Flavobacterales sp.…”

Metagenomic insights into particles and their associated microbiota in a coastal margin ecosystem

“…During nearshore seasonal upwelling events, this salinity intrusion often carries coastal phytoplankton blooms, thereby supplying ocean-derived POM to the lower estuary (Kudela et al, 2005 ; Roegner et al, 2011 ; Herfort et al, 2011a ). Extensive beds of large subtidal kelps (the brown algae Phaeophyta) that are a typical feature of the temperate Pacific Northwest coastline (Schapira et al, 2012 ) also supply POM along the coastal margin.…”

“…Particle-attached bacteria are often observed to be larger than free-living bacteria, likely due to greater substrate accessibility compared to the surrounding waters (Alldredge et al, 1986 ; Simon et al, 2002 ). Many reports also document higher activity on a per-cell basis for particle-attached compared to free-living bacteria (Fandino et al, 2001 ; Grossart et al, 2003 , 2007 ; Schapira et al, 2012 ). Others have, however, noted higher activities in free-living populations (Alldredge et al, 1986 ; Martinez et al, 1996 ; Schapira et al, 2012 ), thus associated environmental parameters and particle properties are likely to be important determinant factors.…”