Edited by: Toshi Nagata, University of Tokyo, Japan
Reviewed by: Mauro Celussi, National Institute of Oceanography and Experimental Geophysics, Italy; Gordon T. Taylor, Stony Brook University, United States
*Correspondence: Federico Baltar
Javier Arístegui
This article was submitted to Marine Biogeochemistry, a section of the journal Frontiers in Marine Science
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Oceanic fronts are widespread features which separate distinct water masses. They are well known to control the distribution of microbial communities in surface waters, although there is scarce information on their role in delimiting critical functions that microbes perform, and on whether their effects can be translated down into the dark ocean. Here we carried out the first study on the variability of hydrolysis of organic matter (extracellular enzymatic activity; EEA) across a permanent front (the Azores Front), coupled with changes in microbial assemblage composition, from the surface down to the bathypelagic zone. The front separated the study area (enclosed into the North Atlantic Subtropical Gyral Province) into two distinct latitudinal sub-regions with sharp differences in the abundance of autotrophic and heterotrophic microbial assemblages, as well as in the extracellular enzymes activities of glucosidases, alkaline phosphatase, and leucine aminopeptidase. South of the front there was an abrupt decline in the abundance of picophytoplankton as well as in heterotrophic prokaryotes with high nucleic-acid content, but an increase in the abundance of prokaryotes with high side-scatter, an indication that cells were growing attached to particles. Concomitantly, there was also an increase in the aminopeptidase to glucosidase ratio, a proxy of higher degradation of proteinaceous material relative to carbohydrates. Interestingly, these sharp changes in microbial assemblages and enzymatic activities north and south of the front were translated down to the deep ocean. Our results suggest that permanent fronts, like the Azores Front, can act as ecological boundaries in the ocean (even within a biogeographical province), in terms of microbial community structure and biogeochemical cycling. Oriented studies on oceanic fronts down to the deep ocean will help to understand how the variability of these widely-extended hydrographic futures will impact microbial communities and carbon cycling in a future ocean affected by trends in global warming, de-oxygenation and acidification.
Microbes are the engines driving oceanic biogeochemical cycles, regulating the composition of Earth's atmosphere and influencing climate (Falkowski et al.,
The most recognized exercise performed in the ocean to set geographical boundaries, in terms of biogeochemical features and the interplay of planktonic systems with regional oceanography, corresponds to Longhurst (
Recent studies have endeavored to define oceanic biomes based on microbial data (e.g., Zwirglmaier et al.,
Here we performed the first study on the variability of organic matter hydrolysis (by looking at EEA), together with the distribution of microbial assemblages, across a permanent front (the Azores Front; AF), from surface to the bathypelagic zone (>1,000 m). EEA are referred as the gatekeepers of the carbon cycle, since, before uptake, microbes need to use EEA to hydrolyze the high molecular dissolved organic matter (DOM) into low molecular weight compounds that can be incorporated (Hoppe,
We hypothesized that, even within a biogeographical province, stable fronts can act as delimiting factor of the dynamics of microbial assemblages, and that the surface boundary effect of the front can be translated down to the dark ocean, providing that the front separates two well-defined regions with different hydrographic and biogeochemical properties.
The AF extends over the eastern North Atlantic subtropical gyre basin, delimiting the northern border of the Azores Current (32–35°N), which is a branch of the Gulf Stream, separating the temperate from the subtropical eastern North Atlantic (Gould,
Hydrographic casts were performed at 69 stations along a latitudinal section crossing the AF, during the CAIBOX cruise, on board the R/V “Sarmiento de Gamboa” from 25th July to 14th August 2009 (Figure
Salinity was measured from samples collected at 2–3 deep levels with a Guildline 8410-A Portasal, in order to calibrate the CTD sensor.
Dissolved oxygen was measured at 15 depths by Winkler potentiometric end-point titration using a Titrino 720 analyzer (Metrohm).
Chl a was estimated fluorometrically by means of a Turner Designs bench fluorometer, previously calibrated with pure chl a (Sigma), following the recommendations of Yentsch and Menzel (
Abundances of autotrophic (
Examples of flow cytometer cytograms (green fluorescence vs. side scatter) from Syto 13-stained heterotrophic prokaryote samples.
The hydrolysis of the fluorogenic substrate analogs L-Leucine-7-amido-4-methylcoumarin, 4-methylumbelliferyl (MUF)- α-D-glucoside, 4-MUF-β-D-glucoside and MUF-phosphate was measured to estimate potential activity rates of leucine aminopeptidase (LAPase), α-glucosidase (AGase), β-glucosidase (BGase), and alkaline phosphatase (APase), respectively (Hoppe,
A hierarchical clustering analysis was performed to produce a dendrogram represented with even spacing (showing the distance between each node as equal), in order to statistically group the sampled stations into regions. We applied the Ward's minimum variance method, where the distance between two clusters is the ANOVA sum of squares between the two clusters added up over all the variables. To reduce the large number of variables to a few principal components, a principal component analysis (PCA) was also performed. Prior to conducting the hierarchical clustering analyses and the PCA, all targeted variables were standardized by subtracting the mean of all values and dividing by the standard deviation of all values (Dauwe and Middelburg,
A detailed characterization of the different water masses observed during the CAIBOX cruise is described in Lønborg and Álvarez-Salgado (
Vertical distributions (0 to 200 m) of
The AF delimits also, at about 200–500 m depth, the confluence of Eastern North Atlantic Central Water (ENACW) from the north with Madeira Mode Water (MMW) from the south. Below the central waters, overflow Mediterranean Water (MW) spreads into the Atlantic, mostly north of the AF, giving rise to a salinity maximum between 600 and 1,400 m depth, while Antarctic Intermediate Water (AAIW), characterized by lower salinity and dissolved oxygen, replaces the MW south of the AF (Figure
Vertical distributions (surface to bottom) of
One of the most interesting patterns of distribution north and south of the front is on beam transmission, which yields a proxy of small suspended particles in the water column. Figure
Recent and past studies support the view that the eastern boundary Canary Current, south of the AF, is a region affected by intense coastal—offshore transport of suspended particles (see Lovecchio et al.,
The picophytoplankton community (
Distribution of the abundances of
Like with picophytoplankton, there are marked changes in heterotrophic prokaryote abundances north and south of the AF in the upper 100 m, more evident in the depth layer from surface down to the DCM (Figure
Distribution of the abundances of
Prokaryotic abundances decrease exponentially with depth to values an order of magnitude lower at 1,000 m than in the upper 100 m, with no significant differences in LNA and HNA assemblages north and south of the AF (Figures
Distribution of the abundances of
The distribution of these HSC prokaryotes, presumably associated with particles, coincides with the region of lower beam transmission south of the AF, indicative of a greater presence of small suspended particles in the water column. This observation adds support to previous studies in the subtropical Northeast Atlantic that ascribe a predominant particle-attached way of life to deep-ocean prokaryotes thriving on suspended particles (Baltar et al.,
Although, there are some reports suggesting similar taxonomic composition of HNA and LNA populations (Servais et al.,
The sharp transition observed for picophytoplankton and heterotrophic prokaryotes across the front is also evident in microbial EEA (Figure
Vertical distributions (surface to 3,000 m) of microbial extracellular enzymatic activities at the biological stations along the sampling section (refer to Figure
Compiling all the biological data together (i.e., the abundance of microbial assemblages and the EEA) along the transect, a clear clustering arises separating the stations north and south of the AF into two regions (Figure
Dendrogram showing the two-way hierarchical clustering of the stations based on the biological data collected (abundance of microbial assemblages and extracellular enzymatic activities). LAPase, leucine aminopeptidase; APase, alkaline phosphatase; AGase, alpha- glucosidase; BGase, beta-glucosidase; Het Prok Abund, total heterotrophic prokaryote abundance; Synecho,
Principal Component Analysis of all the biological data collected in all the stations. Labels like in Figure
There are several potential reasons to explain the shifts in microbial abundances and activities observed at both sides of the front. First, primary production, chlorophyll a and zooplankton biomass have been reported to be higher in the colder waters north of the AF (Riou et al.,
On the other hand, summer is the period of more intense trade winds and consequently higher upwelling activity in the NW African coast, favoring the coastal-ocean transport of organic matter by enhancing both Ekman transport and the development of upwelling filaments (Figure
The results of this study strongly suggest a critical role of the Azores Front (AF) as a border separating two biogeochemically distinct regions. This role is particularly relevant since the AF is a permanent structure (Gould,
Both authors listed have equally contributed to the different aspects of this work including the design, sampling, data analysis, writing and proofing of the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank the captain and crew of the R/V Sarmiento de Gamboa for their support at sea, Gabriel Rosón for the CTD data, C Lønborg and XA Alvarez-Salgado for the chlorophyll data and GJ Herndl for the spectrofluorometer. Thanks also to Josep Coca for providing Figure