Transparent exopolymer particles (TEPs) are a class of gel
particles, produced mainly by microorganisms, which play important roles in
biogeochemical processes such as carbon cycling and export. TEPs (a) are
colonized by carbon-consuming microbes; (b) mediate aggregation and sinking
of organic matter and organisms, thereby contributing to the biological
carbon pump; and (c) accumulate in the surface microlayer (SML) and affect
air–sea gas exchange. The first step to evaluate the global influence of
TEPs in these processes is the prediction of TEP occurrence in the ocean.
Yet, little is known about the physical and biological variables that drive
their abundance, particularly in the open ocean. Here we describe the
horizontal TEP distribution, along with physical and biological variables, in
surface waters along a north–south transect in the Atlantic Ocean during
October–November 2014. Two main regions were separated due to remarkable
differences: the open Atlantic Ocean (OAO,
Transparent exopolymer particles (TEPs) are defined as a class of nonliving
organic particles in aqueous media, mainly consisting of acidic
polysaccharides, which are stainable with Alcian Blue (Alldredge et al.,
1993). They are formed from dissolved precursors that self-assemble to form
TEPs (operationally defined as particles
TEP distribution in marine systems depends on the complex balance between the
sources and the sinks (Alldredge et al., 1998; Passow, 2002a). TEP sinks
include some of the abovementioned processes (sinking of aggregates to the
deep ocean, release to the atmosphere and consumption by organisms), and also
photolysis by UV radiation (Ortega-Retuerta et al., 2009b). Regarding the
sources, TEPs are produced by organisms, mainly microorganisms, during
metabolic and decomposition processes (Hong et al., 1997; Berman-Frank et
al., 2007). Phytoplankton are major TEP producers in the ocean, although
HPs are also able to produce TEPs (Biddanda, 1986; Stoderegger and Herndl, 1998;
Passow, 2002b; Ortega-Retuerta et al., 2010). Some phytoplankton groups that
have been shown to produce TEPs include cyanobacteria (Grossart et al., 1998;
Mazuecos, 2015; Deng et al., 2016); diatoms (Passow and Alldredge, 1994; Mari
and Kiorboe, 1996; Passow, 2002b); dinoflagellates (Passow and Alldredge,
1994); Prymnesiophyceae, including coccolithophores (Riebesell et al., 1995;
Engel, 2004; Leblanc et al., 2009); and Cryptomonads (Kozlowski and Vernet,
1995; Passow et al., 1995). Other organisms such as
TEP sources and sinks in the ocean depend not only on the taxonomic
composition of TEP producers, but they are also influenced by other variables
such as the organism's physiological state (Passow, 2002b), temperature
(Nicolaus et al., 1999; Claquin et al., 2008), light (Trabelsi et al., 2008;
Ortega-Retuerta et al., 2009a; Iuculano et al., 2017b), carbon dioxide
concentration (Engel, 2002), nutrient availability (Guerrini et al., 1998;
Radic et al., 2006), turbulence (Passow, 2000, 2002b), microbe–microbe
interactions (Gärdes et al., 2011) or viral infection (Shibata et al.,
1997; Vardi et al., 2012). For example, limitation by nutrients often
increases TEP production, due to dissolved inorganic carbon overconsumption
(Corzo et al., 2000; Engel et al., 2002a; Schartau et al., 2007), and also
impedes prokaryotic consumption of TEPs (Bar-Zeev and Rahav, 2015). High solar
radiation can stimulate TEP production by
The aforementioned importance of TEPs in carbon fluxes in the pelagic ocean
can be further stressed by considering the following rough numbers: if the
percentage of extracellular carbon release during planktonic primary
production is generally constrained within 10 %–20 % (Nagata, 2000;
Mari et al., 2017), but can reach
Sampling was conducted during the TransPEGASO cruise aboard the Spanish R/V
Hydrographic stations (filled circles) of the TransPEGASO cruise,
sampled during October–November 2014 in the Atlantic Ocean. Chl
TEP concentrations were determined by spectrophotometry following Passow and
Alldredge (1995). Duplicate samples (100–500 mL each) were filtered through
25 mm diameter 0.4
POC was measured by filtering 1000 mL of seawater on precombusted (4 h,
450
Samples for fluorometric Chl
Samples for dissolved inorganic nutrients (nitrate, phosphate and silicate)
were stored in 10 mL sterile polypropylene bottles at
We quantified phytoplankton groups by microscopy. Water was fixed with
hexamine-buffered formaldehyde solution (4 % final formalin
concentration) in a glass bottle, immediately after collection, and then was
allowed to settle for 48 h in a 100 cm
To enumerate picoplankton cells, samples (4.5 mL) were fixed with 1 %
paraformaldehyde plus 0.05 % glutaraldehyde (final concentrations), for
15 min at room temperature, deep frozen in liquid nitrogen and stored frozen
at
Heterotrophic prokaryotic abundance (HPA) was determined by flow cytometry
using the same fixing protocol and instrument as for picoplankton. Before
analyses, samples were thawed, stained with SYBRGreen I (Molecular Probes) at
a final concentration of 10
We used R software packages lmodel2 and ggplot2 (RStudio Team, 2016) to test for covariations and to explore the potential
controlling variables of TEP distribution across the Atlantic Ocean. We
performed pairwise Spearman correlation analyses between TEP and POC
concentrations. We performed bivariate and multiple regression analyses
(ordinary least squares, OLS) between TEP concentrations and several
physical, chemical and biological variables. Data were log transformed to
fulfil the requirements of parametric tests. Ranged major axis (RMA)
regression would have been more suitable since there were errors in both our
dependent and independent variables. However, we decided to perform OLS
regressions for a better comparison of slopes between our study and those
available in the literature. The nonparametric Wilcoxon–Mann–Whitney test
was carried out to compare variables, like TEPs and POC, among regions. Two
main regions were analyzed separately due to remarkable differences in
nutrient, Chl
TEP concentrations ranged from 18.3 to 446.8
Mean, standard deviation and range of temperature (
In the Northeastern Subtropical Gyre and the Canary Current Coastal (stations
1 to 7, Fig. 1) Chl
Variations of sea surface temperature (SST,
The southernmost part of the cruise transect corresponded to the SWAS
(stations 32 to 41). In this region, temperature (7.6–13.9
TEPs and POC covaried significantly and positively across the entire
TransPEGASO transect (Spearman rs analysis,
Average and standard deviation of the contribution of TEP, phytoplankton and HP to the POC pool (%) in the OAO and the SWAS.
TEPs were significantly and positively related to Chl
Across the whole transect, TEPs presented a significant (
Relationship between the 24 h-average (previous to sampling) solar
irradiance (W m
Review of open-ocean surface TEP concentrations (mean and ranges;
We present the first distribution of surface (4 m) TEP concentration along a
latitudinal gradient in the Atlantic Ocean, covering both open sea and shelf
waters. It is worth mentioning that vertical variability within the top
surface meters (
We found maximum TEP concentrations in the regions with high nutrient supply,
namely in the station located in the CU and within the SWAS. Ours are the
first TEP concentrations ever measured in the SWAS (Table 1), and only three
more studies have reported TEP concentrations in coastal or shelf waters of
the Atlantic Ocean (Harlay et al., 2009, 2010; Jennings et al., 2017). The
SWAS is a high-nutrient region due to the arrival of cold nutrient-rich
subantarctic water with the Malvinas Current. This current collides near
40
The significant positive correlation between TEPs and POC observed in our
study highlighted the importance of TEP-determining POC horizontal variations
in the surface Atlantic Ocean, suggesting a high contribution of TEPs to this
pool. A few values of TEP–C%POC were unrealistically higher than
100 %, a feature that has also been observed in other studies (Engel and
Passow, 2001; Bar-Zeev et al., 2011; Yamada et al., 2015). This suggests the
inaccuracy of the use of standard TEP-to-carbon conversion factors (CFs,
0.51
All in all, our results clearly show that TEP–C constituted an important
portion of the POC pool in the Atlantic Ocean (from 28 % to 110 %).
This contribution is comparable to that reported in the eastern Mediterranean
Sea (Bar-Zeev et al., 2011; Parinos et al., 2017), lower than in the western
Arctic (Yamada et al., 2015), but higher than in the northeastern Atlantic
Ocean (Harlay et al., 2009, 2010). Both in the OAO and SWAS, TEPs comprised
the largest share of the POC pool, with phyto–C being equal or the second
most important contributor to POC (Fig. 3). Phyto–C surpassed TEP–C in only
one station in the SWAS. The contribution of phyto–C and HP–C to the POC
pool should be considered with caution, as the glass
fibre filters (nominal pore size 0.7
A previous study in a eutrophic system reported TEP–C as the dominant POC contributor (Yamada et al., 2015), whereas others found that phyto–C represented the largest share to POC compared to TEP–C and HP–C (Bhaskar and Bhosle, 2006; Ortega-Retuerta et al., 2009b; de Vicente et al., 2010). With our results taken all together, we hypothesize that in oligotrophic conditions TEP–C is the predominant POC fraction, because nutrient limitation favors TEP production by phytoplankton and limits TEP consumption by bacteria. Conversely, in eutrophic conditions, the predominant POC fraction depends on many variables like the community composition, the bloom stage and sources of TEPs other than phytoplankton.
Regression equations and statistics describing the relationship
between TEP and different variables throughout the TransPEGASO cruise (note
all variables were log
In order to better understand and even predict the occurrence of TEPs in the surface ocean, it is important to describe their distribution together with those of their main putative sources (phytoplankton and heterotrophic prokaryotes), sinks and environmental modulators, across large-scale gradients. However, most of the previous studies of TEPs in the Atlantic Ocean were restricted to local areas, and, to our knowledge, only one included a complete description of these variables together in a long transect (Mazuecos, 2015).
Our dataset suggests that phytoplankton is the main driver of TEP
distribution in the surface Atlantic Ocean at the horizontal scale, since
significant positive relationships were observed between TEPs and both Chl
Relationship between TEP and Chl
Results of multiple regression analyses between TEPs and combined
variables, all log
In the OAO, the phytoplankton groups that showed a significant (
The oligotrophic ocean covers a big portion of the global ocean and it is
mostly dominated by picophytoplankton (Agawin et al., 2000), chiefly
In the SWAS, unlike in the OAO, the significant relationship between TEPs and
the total phytoplankton biomass (
Regarding the influence of abiotic factors in TEP distribution, we found a
negative relationship (
The role of HPs as potential drivers of TEP distribution is not
straightforward, since their net effect on TEP accumulation depends on local
conditions. Across the entire transect, TEP concentration was significantly
(
In summary, our study describes for the first time the horizontal
distribution of TEPs across a north–south transect in the Atlantic Ocean.
TEPs constituted a large portion of the POC pool, larger than phytoplankton at
most stations and always larger than heterotrophic prokaryotic biomass. This
supports the important role of TEPs in the carbon cycle. The drivers of TEP
distribution were primarily phytoplankton and, to a lesser extent,
heterotrophic prokaryotes among sources, with
Data are not publicly accessible yet. For further information, please contact the corresponding author.
MZ conducted the field work, analyzed samples, and processed and analyzed the data. EOR and RS designed the study and analyzed data. SN, PRR, ME and MMS analyzed samples and provided data. MD helped with data contextualization. MZ, EOR and RS wrote the paper with the help of all co-authors.
The authors declare that they have no conflict of interest.
This research was funded by the Spanish Ministry of Economy and
Competitiveness through projects PEGASO (CTM2012–37615) and BIOGAPS
(CTM2016-81008-R) to Rafel Simó. Marina Zamanillo was supported by a FPU
predoctoral fellowship from the Spanish Ministry of Education and Culture.
Eva Ortega-Retuerta was supported by a Marie Curie Actions Intra-European
Fellowship (H2020-MSCA-IF-2015-703991). The authors thank Pep Gasol and
Carolina Antequera for assistance with flow cytometry; Maximino Delgado for
microscopic phytoplankton counts; Rocío Zamanillo and Rafael Campos for
assistance with R software; and the scientists, the Marine Technology Unit
(UTM–CSIC) and crew on board the R/V