The global marine biogeochemical cycle of aluminium (Al) is believed to be
driven by marine diatoms, due to the uptake of dissolved Al (DAl) by living
diatoms from surface seawater. The occurrence of Al in diatom biogenic
silica (BSi) can inhibit the dissolution of BSi, thus benefiting the effects
of the ballast role of diatoms in the biological pump and forming a coupled
Si–Al biogeochemical cycle. However, the occurrence characteristic of Al in
marine diatoms is still unclear. In particular, whether or not Al is
incorporated into the structure of BSi of living diatoms is unrevealed,
resulting in difficulties in understanding the biogeochemical behaviours of
Al. In this study,
Aluminium (Al) is the most abundant metal element in the Earth's crust, and
it mainly occurs in Al-bearing minerals such as aluminosilicate (Taylor, 1964).
The weathering of such aluminosilicates results in a huge carbon (C) sink in
rocks and soils due to the transformation of CO
Due to its lack of an essential biological role (even toxicity) (Xie et al., 2015; Gillmore et al., 2016), the terrestrial cycling of Al is believed to be primarily controlled by inorganic processes. However, marine diatoms are found to take up and incorporate Al into their cells (Q. Liu et al., 2019). Diatoms can eliminate plenty of DAl from surface water when they bloom (Hall et al., 1999; Ren et al., 2011), and they export Al into the sedimentary layers through the sedimentation of post-mortem diatoms, forming a coupled Si–Al biogeochemical cycle in the oceans (van Hulten et al., 2014).
Diatoms are a type of widely distributed single-cell algae in the oceans,
and they account for up to
Compared with other marine phytoplankton, diatoms are more effective at carbon sequestration over longer timescales due to their frustules, which are composed of biogenic silica (BSi) with high mechanical stability (Baines et al., 2010). Since it acts as a ballast (De La Rocha et al., 2008; Honda and Watanabe, 2010), BSi carries the OC to deeper oceans and deposits on the seafloor, forming a coupled Si–C cycle.
Considering the key role of diatoms in carbon sequestration, the Al in diatom cells is also involved in the C cycle in the oceans, and thus, Al participates in the global C geochemical cycle through inorganic and biological processes (Gehlen et al., 2002, 2003; Ren et al., 2013). Although preliminary studies have been carried out to investigate the Al in freshwater (D. Liu et al., 2019) and marine diatoms, the occurrence of Al in marine diatoms is far away unclear, which results in difficulties in understanding the abovementioned diatom-derived Al cycle.
That Al is incorporated into the organic components, and BSi of diatoms has been studied. For organic components, the occurrence mechanism and distribution have been well described (Q. Liu et al., 2019). For BSi of marine diatoms, the coordination of Al in BSi was identified by using X-ray absorption spectrometry (XAS) and nuclear magnetic resonance (NMR) spectroscopy, showing Al with tetrahedral coordination (Beck et al., 2002; Gehlen et al., 2002; Koning et al., 2007; Machill et al., 2013). However, the information of this Al, including its content and distribution characteristics, is lacking. Moreover, the previous evaluation cannot avoid the interference of the Al from organic components of diatoms and Al-bearing minerals. For the former, the high activity of fresh BSi results in the easy adsorption of DAl from Al-containing solutions during the removal of the Al-bearing organic components of diatoms, which interferes with the evaluation of the structural Al (Moran and Moore, 1988; Koning et al., 2007). For the latter, Al-bearing tiny mineral particles can hardly be excluded from sedimentary BSi even with the greatest of care, e.g. the acid washing reported by Gehlen et al. (2002). Due to these challenges, the characteristics of Al in the marine BSi structure are still unclear, although possible contents and coordinated states have been proposed. The reason that so much attention has been paid to the structural Al in BSi is that structural Al has a dissolution–inhibition effect on BSi. About 25 % decrease in the solubility of BSi was shown when Al substitutes for 1 out of every 70 Si atoms (Dixit et al., 2001), and thus, structural Al is believed to be one of the key factors that influence the transfer of BSi from the surface ocean to pelagic sediments. Therefore, the indefinite occurrence characteristics of Al in BSi severely limit our understanding of the composition, structure, and water stability of BSi.
In this study, a widely distributed marine diatom in marginal seas,
Phylogenetic trees of diatom strains isolated from the culturing diatoms. The scale bar indicates the number of substitutions per site for a unit branch length.
The diatoms were cultured in artificial seawater supplemented with
Trace-metal clean processes were used to eliminate the interference from
other elements. Before the cultivation experiment, all of the bottles and
tubes were soaked in 10 % hydrochloric acid for 24 h, sterilized at
120
AlCl
After 14 d of culturing, the diatoms were collected through high-speed
centrifugation at 11 000 rpm. The obtained diatoms (Fig. 2) were rinsed with
deionized water three times to remove any impurities adsorbed on the
surface. The solid obtained was freeze-dried after centrifugation. Two
pretreatment procedures were used to remove any Al adsorbed on the surface
of the diatoms and their organic components to obtain pure BSi: (1) immersion
in 0.05 M EDTA for 12 h followed by washing three times and (2) immersion in
30 % hydrogen peroxide solution for 48 h followed by washing five times.
The removal of the organic components was confirmed using a Vario EL III
elemental analyser with a detection limit of
Scanning electron microscopy (SEM) images of
The FIB milling was carried out using FIB scanning electron microscopy (SEM;
FEI Helios Nano Lab 450S) equipped with a flip stage, an in situ scanning
transmission electron microscope (STEM) detector, a Tomahawk ion column, and
a multichannel gas injection system. For the FIB milling conducted to obtain
a thin BSi slice, a single frustule of BSi selected for characterization was
picked using a nanomanipulator (Oxford OmniProbe 400), and a 5 kV focused
gallium ion (Ga
In previous studies, the change in the Al concentrations of the culture
medium was used to evaluate the Al uptake of diatoms. However, some of the
Al forms a new Al-bearing phase based on changes in the chemical environment
(such as reverse weathering) (Isson and Planavsky, 2018), rather than being involved in the
biological processes of diatoms. To avoid the disturbance of such Al, which
does not incorporate into the cells of the diatoms, the
The data for the specific growth rate and EDS spot analysis were obtained on
the basis of the mean
To investigate the influence of Al on the growth of
The cell densities of the diatoms cultured in culture mediums with (Al-added) and without (Al-free) the addition of Al during the 14 d culturing period.
FIB milling can remove the external surface of the diatom and impurities
adsorbed onto it, allowing for the detection of the inner structure of the
BSi. Thus, the subsequent EDS detection obtains the structural element
distributions of the BSi. In this case, the combined FIB–EDS analyses could
detect the structural elements of BSi and avoid the disturbance of the
non-structural elements (those adsorbed on the external surface of BSi). The
(
This is direct evidence of the presence of Al in the internal surface of BSi
sourced from living marine diatoms, demonstrating the occurrence of
structural Al in the diatomaceous biological framework of marine diatoms.
The Al is incorporated into the BSi and used to build diatom BSi. Based on
the EDS mapping analysis, the average
More than 300 spots on diatoms and their BSi were analysed using EDS, and
the average
The scavenging of Al from seawater by diatoms has been widely observed during diatom blooms (Hall et al., 1999; Ren et al., 2011). This unique behaviour of Al uptake has attracted a great deal of attention, and a corresponding biogeochemical Al cycle driven by diatoms was hypothesized (van Hulten et al., 2014). Proving the occurrence of Al in diatoms is key to understanding the mechanism of Al uptake by marine diatoms. Q. Liu et al. (2019) investigated Al incorporation into diatoms and proposed the distribution and the content of Al in the organic components of diatoms based on various extraction methods (Q. Liu et al., 2019). Occurrence of Al in BSi has been investigated (Beck et al., 2002; Gehlen et al., 2002; Koning et al., 2007; Machill et al., 2013). The coordination characteristic of Al in BSi which was obtained from living diatoms and sediments was evaluated using the Al K-edge X-ray absorption near-edge structure (XANES) spectroscopy and NMR spectroscopy (Beck et al., 2002; Gehlen et al., 2002; Koning et al., 2007), showing Al with tetrahedral coordination in BSi. Therefore, the coupled Si and Al biogeochemical cycle in oceans was proposed based on these results. However, the distribution and content of structural Al in BSi of marine diatoms was still not well-known.
During the evaluation of Al in BSi, avoiding the interference of the Al in organic components of diatoms and in Al-bearing minerals loading on the surface of BSi in sediments is very difficult. Removing organic components of diatoms could release Al, and some Al would be adsorbed by the fresh BSi which possesses the high activity (Koning et al., 2007). Moreover, sedimentary BSi contained plenty of Al-bearing tiny mineral particles which are hardly removed by physical and chemical pre-treatments (Michalopoulos et al., 2000; Gehlen et al., 2002; Koning et al., 2007). The two types of Al influence the detection of the Al incorporated in the BSi, preventing the identification and quantification of the structural Al. Due to these problems, the Al detected through elemental analyses such as X-ray fluorescence (XRF), and inductively coupled plasma optical emission spectroscopy (ICP-OES) for the DAl in diatom culture medium (de Jonge et al., 2010; Machill et al., 2013), and EDS for marine BSi is difficult to evaluate structural Al content and even to identify its occurrence.
In our previous study, we found that FIB milling allowed us to obtain a
slice of an internal section of BSi and to remove the external surface,
avoiding the disturbance of any impurities in the further detection of the
structural elements (D. Liu et al., 2019). The freshwater BSi was investigated to reveal
Al occurring in the structure of BSi and a high-level concentration of Al
was detected. Through a combination of FIB and EDS, direct and visible
evidence was obtained, illustrating the distribution and quantity of the
structural Al in BSi. Structural Al was observed in BSi of marine diatoms,
demonstrating that marine diatoms take up Al and use it to build their
siliceous framework (BSi). Similar to freshwater diatom BSi, Al shows
similar distribution characteristics to Si in marine BSi, but the Al content
of marine diatoms (
Moreover, structural Al is proposed to have a dissolution–inhibition effect
on BSi, i.e. a 25 % decrease in BSi solubility when Al substitutes for 1
out of every 70 Si atoms (
In this study, the occurrence characteristics of structural Al in BSi of
marine diatoms,
The data generated for this study are available on request to the corresponding author.
The supplement related to this article is available online at:
QT and DL designed the experiments and wrote the manuscript. HW and ML were collected the samples of marine diatoms. QT and JZ carried out the culture of diatoms and EDS analysis. PY and WY were involved in the discussion on the data analysis and revision of the draft. DL, JZ, and HG were involved in the FIB analysis.
The contact author has declared that neither they nor their co-authors have any competing interests.
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This work is supported by the National Natural Scientific Foundation of China (grant nos. 42172047 and 41772041), the funding of State Key Laboratory of Marine Environmental Science (MEL) Visiting Fellowship of Xiamen University (MELRS2006 grant), Jiangxi Province technology innovation guidance project (grant no. 20212BDH81036), and Science and Technology Planning Project of Guangdong Province (grant no. 2020B1212060055). This is a contribution (grant no. IS-3134) from GIGCAS.
This research has been supported by the National Natural Scientific Foundation of China (grant nos. 42172047 and 41772041), the funding of State Key Laboratory of Marine Environmental Science (MEL) Visiting Fellowship of Xiamen University (MELRS2006 grant), Jiangxi Province technology innovation guidance project (grant no. 20212BDH81036), and Science and Technology Planning Project of Guangdong Province (grant no. 2020B1212060055).
This paper was edited by Anne Marie Tréguier and reviewed by two anonymous referees.