Silicon https://doi.org/10.1007/s12633-018-9809-0
ORIGINAL PAPER
Diatom Frustules Nanostructure in Pelagic and Benthic Environments A. Leynaert1 · C. Fardel1 · B. Beker1 · C. Soler1 · G. Delebecq1 · A. Lemercier1 · P. Pondaven1 · P. E. Durand2 · K. Heggarty3 Received: 25 August 2016 / Accepted: 16 March 2018 © Springer Science+Business Media B.V., part of Springer Nature 2018
Abstract Diatoms are an important group of eukaryotic microalgae with a siliceous cell wall, the frustule. Diatoms are traditionally subdivided into two sub-classes, namely centric diatoms with a radial symmetry and pennate diatoms with a bilateral symmetry. These two groups of diatoms have usually biotope “preferences”, with centric diatoms dominating the pelagic environments, whereas the benthic habitats are mostly inhabited by pennate diatoms. The question of how the morphology of diatoms (centric versus pennate) or the ultrastructure of the frustule could be driven by ecological constrains remains unclear. For example, some studies have suggested that the structure of the diatom frustule could play a role in the light harvesting performances. In this work, we studied the variations of the diatom frustules nanostructure in several benthic and pelagic species inhabiting the same coastal ecosystem, particularly the ultrastructure that includes the distribution and size of the frustule pores. Although the species studied here experience different ecological constrains in term of light, we found no significant differences between benthic and pelagic species, in either the size of the pores (average = 285 (± 108) nm) or the distance between them (average = 234 (± 87) nm). Moreover, the intra-species variability was sometimes larger than the variability observed between cells from different genera. We concluded that the pore morphometry is controlled by a combination of genetically-driven processes of bio-mineralization, and episodic variations in environmental growth conditions which influence the chemical precipitation of silica within the cells. Keywords Bacillariophyta · Benthic and pelagic diatoms · Microphytobenthos · Frustule structure · Silicification · Biomineralization · Light
1 Introduction About 10,000 to 12,000 species of diatoms are described in the literature. Diatoms are unicellular but could also be colonial [1, 2]. Their size varies between 2 μm and 2 mm but they mainly represent the microplanktonic classes ranging between 20 and 200 μm. Based on their different morphologies, diatoms are divided into two subclasses: the pennate A. Leynaert
[email protected] 1
Laboratoire des Sciences de l’Environnement Marin (LEMAR), UMR CNRS 6539, Institut Universitaire Europ´een de la Mer (IUEM), Technopˆole Brest-Iroise, 29280 Plouzan´e, France
2
Laboratoire de Biotechnologie et Chimie Marine (LBCM), EA 3884, Centre de Recherche C. Huygens, Universit´e de Bretagne Sud, BP 92116, 56321 Lorient Cedex, France
3
D´epartement d’Optique, Telecom Bretagne, Technopole Brest-Iroise, 29280 Plouzan´e, France
(bilateral symmetry) and the centric (radial symmetry) [3]. In marine environments, they colonize all habitats depending on light availability Centric diatoms are mostly pelagic, while the pennates belong mainly to the microphytobenthos, i.e. microalgae growing on the seabed in shallow areas [4]. A one year-long survey, conducted in the Bay of Brest in order to study the seasonal dynamics of pelagic and subtidal benthic micro-algae, has shown that at 10 m depth benthic diatoms were able to produce as much biomass as the overlying micro-algae [5]. This result suggests a good growth adaptation at such depth, knowing that benthic diatoms receive on average ten times less light than at the surface [5]. However, the mechanisms behind the differences in the ecophysiology of benthic and pelagic diatoms and their adaptation to these different environmental conditions remain unclear. Regardless of their habitat preferences, diatoms share the feature of having a silica exoskeleton as a cell wall, called the frustule. The frustule is formed by two almost identical valves ornamented on their surfaces with micro- and
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nano-structures (such as striae, punctures, areolas, etc) with extremely regular yet variable patterns that depend on the species. The complexity of the frustule structure raises the question of its interest to the diatoms at the ecological and/or physiological levels. It has been suggested that the complex structure of the frustule may present different advantages such as a mechanical protection for the cell [6] an armor against predators [7], an effective pH buffer [8], or an improvement to nutrient uptake in patchy environments [9]. Another study has suggested that due to its periodic pattern at the scale of the visible wavelengths, the diatom frustule could present peculiar optical properties [10]. Other studies have shown that the morphology and nanostructure of the diatom’s silicified cell wall can be affected by changes in the environmental conditions, such as nutrient availability [11] or the quality of light [12]. Here, we investigate whether some aspects of the frustules morphology could be markedly different in pelagic and benthic diatoms. We analyze the micro- and nano- structures of two diatom communities growing in contrasted environmental conditions: the pelagic species and the subtidal benthic species, sampled at different period of the year in the same ecosystem. We then focus on the diameter and distribution of the circular pores that ornament the outside valves of the frustule.
2 Materials and Methods 2.1 Sampling The sampling took place during a survey that was conducted in 2011 at Lanv´eoc site (48◦ 17 41 23 N–4◦ 27 12 .63 W), a temperate ecosystem located in the Bay of Brest, (Northeast Atlantic) (Fig. 1). The Bay of Brest (180 km2 ) is a shallow marine semi-enclosed bay with more than 50% of Fig. 1 Geographical locations of the Bay of Brest and the study site
its total area below 5 m of depth. The bay is a macrotidal system affected by average tide amplitude of 4 m. The water column is generally well mixed due to the presence of a strong tidal current and surface wind stress [13]. The sampling was carried out once a week from the beginning of February to the end of October 2011, aboard the Research vessels “Hesione” or “Albert Lucas”. The water samples dedicated for a set of chemical analyzes and for the pelagic diatoms examination were collected with a 12 L Niskin bottles at two depths (surface and bottom). The benthic diatoms were examined from a series of Plexiglas plates (12 × 15 cm). The plates were placed on the sea bottom (10 m of depth) at the site of sampling six months before the start of the survey. They were used to simulate an artificial hard surface substratum that offers the opportunity to study the samples in situ rather than culture samples that may generate biases.
2.2 Physical Measurements Across the water column, measurements of salinity, temperature and photosynthetically active radiation (PAR) were conducted weekly using a CTD profiler Sea-Bird SBE-911, equipped with a PAR (μmol photons m−2 s−1 ) sensor. The PAR was also measured with a multispectral radiometer RAMSES (Radiation Measurement Sensor with Enhanced Spectral Resolution) with 1 nanometer resolution at the wavelength range between 400 and 700 nm. The latter measurement was run at different depths: the sub-surface, 1 m, 3 m, and at the bottom.
2.3 Chemical Parameters The water samples dedicated for nutrient analyzes were filtered on Nuclepore membrane filters (0.6 μm) immediately in the lab after the sampling procedure. The samples for
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measurements of dissolved inorganic nitrogen (NO3 /NO2 ) and phosphate (PO4 ) were thereafter frozen, whereas samples for silicilic acid (Si(OH)4 ) were stored at 4 ◦ C in the dark. The concentration of each chemical compound was later measured by colorimetric methods on a Technicon Auto-Analyzer II [14, 15].
2.4 Sample Conservation and Examination Under an Optical Microscope The samples were fixed with Lugol’s solution and then an identification to the lowest possible taxonomic level of the cells was performed using the Uterm¨ohl method with multiple magnifications (10×, 20× and 40×) under an inverted optical microscope (Zeiss Axio).
2.5 Preparation of Diatom Frustules for SEM Examination and Pictures Processing In order to improve the observation quality of the morphological structure of the frustule with a scanning electron microscope (SEM), the samples were oxidized to remove the cell content and the organic material around the shell. This procedure can be performed in many ways [16–18], such as the quantity of hydrogen peroxide added to the sample, or the time allowed for the digestion adjusted depending on
Fig. 2 a SEM images of pelagic and benthic diatom frustules, b measurement by image analysis of the distance between pores (small red bares) and the pores surface (colored dots)
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the objective of the study. In this study, full attention was given to alter as little as possible the structure of the diatom frustules, while losing as few diatoms as possible. This is particularly important when working with natural samples because cells are much less abundant than in cultures. Moreover, some species do not show the same tolerance to the chemical treatments. The best way to remove gently the organic matter from the frustules is to process the samples with hydrogen peroxide at 50%, followed by incubation at 55 ◦ C for 1 to 2 h. After removing the organic matter, the samples were cooled in a water bath before being filtered very slowly on a Nuclepore filter (5 μm pore size). Thereafter, the filters were dehydrated with alcohol solutions with increasing concentrations, then placed in a petri dish and stored in the oven (at 50 ◦ C) until the analysis. Cleaned diatom frustules were mounted on a microscopy stub and coated with a gold/palladium layer. The stubs were then observed using a scanning electron microscope (FEI Quanta 200 SEM). Some pictures of the diatom frustules were taken depicting the entire frustule when possible, and pore arrangements on representative parts of the frustules. The resulting images were processed with the picture processing software Visilog 5.4 (ed. Noesis). The measurements take into account the spacing between each pore, from one edge to another, as well as their diameter and surface (Fig. 2).
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2.6 Statistical Analysis The statistical analysis was performed with the StatSoft software (2011). The values used are the mean and standard deviation. Two non-parametric statistical tests were used: –
–
The Mann-Whitney test that determines whether two independent groups come from the same population and whether the number of observations in the groups may differ. This test was used to check the hypothesis (H), which stipulates that significant difference exist between the two groups, benthic and pelagic species. The Kruskal-Wallis test was used to determine whether several independent groups come from the same population. The groups may have different numbers. The hypothesis (H) used was that inter-pores distance or pore diameter do not differ within a given population.
For both tests, we consider that the hypothesis H is rejected if p ≤ 0.05, where p is a critical probability.
3 Results
study. The other pictures depicted damages on the frustules that may have occurred during sample preparations, or the cells presented anomalies such as frustules lacking details (case of Chaetoceros spp) or having pores with unmeasurable forms.
3.2 Cells Size The variety of shapes of diatom species makes them hardly comparable in term of size. Therefore, we measured linear dimensions (length, width) and used standardized equations based on their geometric shapes [19] in order to assess the frustules surface and volume. The pelagic species found in our samples were much smaller compared with the benthic species (Table 1). The difference was more noticeable when comparing the length of the pelagic cells (7–24 μm) with the length of the benthic cells (8–250 μm, i.e. 10-fold difference for the longest one). The difference between the two groups weakened when considering the cell surface (190–2262 μm2 for pelagic and 20– 3200 μm2 for benthic, i.e. 1.4 fold) or the cell volume (284– 10,857 and 236–25,000 μm3 , respectively for pelagic and benthic species, i.e. 2.3-fold difference for the biggest one).
3.1 Diatom Diversity 3.3 Pore-to-Pore Distance Throughout the year of our survey, we enumerated a total of 18 genera among pelagic diatoms. The diatom community was chiefly dominated by Chaetoceros spp and Thalassiosira spp. During the bloom period, species such as Dactyliosolen fragilissimus and Cerataulina pelagica appeared, yet Chateoceros spp. were still dominant. After the bloom, other species arose like Guinardia delicatula whereas Leptocylindrus danicus and Pseudonitzschia spp. were observed intermittently from early to end of the spring. For the benthic community, a total of 23 genera were observed during the survey, all of them, except Nitzschia, were different from those found in the water column. Right from the start of the season, genus like Fragilaria and Navicula dominated the benthic community and were present throughout the survey. In early spring, Cocconeis, Pleurosigma, Toxarium were observed whereas Amphora, Licmophora, Achnanthes, appeared during the bloom. After that, only Navicula, Fragilaria, and Cocconeis appeared frequently, while genus like Nitzschia, Pleurosigma, and Amphora appeared intermittently through the rest of the year. All pelagic species observed during the survey were with radial symmetry (centric diatoms), except Pseudonitzschia spp, whereas within the benthic, all species encountered were with no exception axisymmetric (pennate diatoms). Among all the species observed under the optical microscope, 29 were recovered and identified under SEM. Yet only 18 of them (13 genera), well-preserved cells, permitted to acquire SEM images of sufficient quality to be used in this
The average distance between pores of the diatom frustules was calculated for each pelagic species (Fig. 3, Table 1). The pore-to-pore average distance varied between 168 nm (centric diatom) and 388 nm (Thalassiosira cf conferta). Two species showed higher standard deviations among cells: Thalassiosira cf conferta and Thalassiosira gracilis. The applied Kruskal-Wallis test indicated that there were significant differences between species within the pelagic diatom community. For the benthic diatoms, the average distance between pores varied between 72 nm (Cymbellonitzschia szulczewskii) and 345 nm (Licmophora sp.). The calculated standard deviations were quite small except for some genera such as Navicula and Nitzschia According to the Kruskal-Wallis test, significant differences may be found in these measures (p = 0.001). The comparison between the two diatom groups (benthic and pelagic) did not show a significant difference according to the Mann-Whitney’s test (p = 0.089). Based on our results, the overall average distance between pores was 234 (± 87) nm, all species considered in both benthic and pelagic diatoms.
3.4 Pores Diameter The measured diameters of pores varied between 108 and 515 nm (Fig. 4, Table 1). The average diameter for benthic diatoms pores varied between 108 nm (Amphora sp.) and
Silicon Table 1 Parameters measured on diatom frustules. SD is Stantard Deviation Genus/Species
Number of Number of Length Surface Biovolume Average distance SD Average pore SD cells analyzed measurements (μm) (μm2 ) (μm3 ) between pores (nm) diameter (nm)
Pelagic Centric diatom Minidiscus sp. Tryblionella Thalassiosira cf conferta Thalassiosira gracilis Thalassiosira punctigera Thalassiosira sp. Thalassiosira tenera Benthic Amphora sp. Synedra sp, Cocconeis sp. Cymbellacea sp. Cymbellonitzschia szulczewskii Grammatophora sp. Licmophora sp. Navicula sp. Nitzschia sp. Tabularia sp. Toxarium hennedyanum
4 2 2 11 6 6 12 2 2 5 22 3 3
420 118 88 151 319 517 682 126 92 132 411 86 58
8,5 7 21 16 16 14 17 24 13 250 14 25 8
190 192 509 1 005 603 418 1 081 2 262 291 3 200 223 244 20
284 269 1 188 3 217 1 608 924 3 632 10 857 500 25 000 330 302 236
168 169 280 388 353 183 174 331
9 40 50 89 158 13 53 26
137 291 194 72
23 89 45 6
5 2 7 3 14 13
220 249 93 180 158 267
18 75 22 20 35 235
405 1 679 515 322 242 2 654
848 2 600 1 106 550 560 16 356
201 345 227 292 149 251
62 15 129 134 79 98
146 263 397 381 241 204 240 515 108
63 233 199 231 165 98 147 436 92
385
167
265
119
338
107
270 240
130 159
In the upper part, the pelagic species and in the lower part the benthic species. The number of cells analyzed and the number of measurements are also given
385 nm (Cocconeis sp.). The standard deviations were small but the Kruskal-Wallis test (p = 0.045) showed a significant difference between these measurements. For pelagic diatoms, the average diameter of pores varied between 146 nm (centric diatom) and 515 nm for Thalassiosira tenera but with a very large standard deviation. The Kruskal-Wallis
test showed a significant difference (p = 0.002) between species within the pelagic community. Comparing the pelagic and benthic communities using the Mann-Whitney’s test showed no significant differences between the two groups of diatoms (p = 0.947). Based on our results, the average diameter of pores for all species considered was 285 (± 108) nm.
Tabularia sp. Navicula sp.
Diatom genera
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Grammatophora sp. Cymbellacea sp. Synedra sp, Thalassiosira sp. Thalassiosira gracilis Tryblionella Psammodiscus nidus 0
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Average distance between pores (nm)
Fig. 3 Average distance between frustule pores (in nm) for benthic (gray bars) and pelagic (hatched bars) diatoms
Toxarium hennedyanum Tabularia sp. Navicula sp. Grammatophora sp. Cocconeis sp. Amphora sp. Thalassiosira tenera Thalassiosira sp. Thalassiosira puncgera Thalassiosira gracilis Thalassiosira cf conferta Tryblionella Minidiscus sp. Psammodiscus nidus 0
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Fig. 4 Average frustule pores diameter (nm) for benthic (gray bars), and pelagic (hatched bars) diatoms
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3.5 Environment Variables In the Bay of Brest, seawater temperatures vary between 8.7 ◦ C in February and 17.4 ◦ C in August (Fig. 5a). The interpretation of the CTD profiles indicated a recurrent wellmixed water column, with an amplitude of about 0.7 ◦ C between the sea surface and the sea bottom throughout the year.
a)
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Temperature (°C)
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Fig. 6 Spectral distribution and vertical decrease of the down-welling irradiance at the sampling station measured at 0, 1, 3 and 11.5 m depths
14 12
Surface Boom
10 8
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800 600 400 200 0
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35 Surface DIN
30 Concentraon (μmol L-1)
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Across the water column, the irradiance decreases from the surface to the seabed (Fig. 5b). Throughout the year of survey, the coefficient of extinction (k) across the water column was estimated between 0.38 and 0.11 m−1 . Sea surface irradiance (0.1 m depth) was reported to follow a seasonal pattern [5] with the minimum recorded in February (3.2 mol-photon m−2 day−1 ) and the maximum in May (58.3 mol-photon m−2 day−1 ). Our results showed that in average, 12% of surface irradiance reached the seafloor (10 m depth). The attenuation of light is also dependent on the wavelength ranges. Figure 6 shows in the Bay of Brest the spectrally resolved irradiance measurements performed at different water depths from surface to bottom: 0 m, 1 m, 3 m and 11 m. At each depth, the maximum irradiance spectra peaked consistently around 550 nm. However, the light intensity did not peak at any given wavelength for the surface spectrum. It rather extended over a wide wavelength window, between 500 and 700 nm. We noticed, a rapid loss with depth of the red wavelengths (around 700 nm). Consequently, blue and green wavelengths became dominant at depth (Fig. 7). Our results showed that the water column was highly enriched with nutrients from mid-January until early March, with a peak of increase around mid-February (Fig. 5c). The
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0.00 350
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Wave lenght (nm) Fig. 5 Seasonal evolution of a dissolved inorganic nitrogen (DIN) and silicic acid (DSi) concentrations, b temperature and c light, at the surface water and on the seabed in the study site
Fig. 7 Light attenuation coefficient (K, in m−1 ) between the surface and 10 m depth, as a function of wavelength (nm)
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maximum concentrations reached 34 μmol L−1 for DIN and 17 μmol L−1 for DSi. The latter became completely depleted at the beginning of May but it rose again in a week time and continued rising until October. The concentrations of DIN depleted steeply from March until mid-May and remained at a minimum until the end of August. Apart from a few exceptions, we noticed no marked difference in nutrient concentrations between the surface and bottom water.
Pore diameter
Distance between pores 0
100
200
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nm
Fig. 8 Total ranges of pore diameters (nm) and pore-to-pore distances (nm)
4 Discussion and Conclusions 4.1 Pore Architecture of Pelagic and Benthic Diatom Frustules Among the characteristics used in taxonomy the number of pores per unit of length is commonly considered [20], but neither the pore diameters nor the pore-to-pore distances are constantly mentioned. To our knowledge, our study is a first study that evaluate the variation ranges of the architecture of pores in diverse diatoms species sampled in situ. Furthermore, our study considered species from contrasted biotopes, the pelagic and benthic. Our study focuses first on the variability observed in the pore architecture within the same species as in the case of the distance between the pores in Thalassiosira gracilis (353±158 nm, Fig. 3), or the pore diameter in Thalassiosira tenera (515 ± 436 nm, Fig. 4). The variability is quite important if we consider that it can be of the same order of magnitude as the fluctuations observed at a genus level. The variations in the size of pores have already been reported for Coscinodiscus granii [13] in controlled growth conditions. However, the reported changes in the pore nanostructures were sometimes larger than the variations observed in different growing conditions, which disagree with the belief that diatom cell wall structure is species specific. This concept, in turn, contradicts with the method that uses pores distribution in the diatom species determination. The pore nanostructure variations are particularly considerable in some genera like Navicula and Nitzschia. The variations of pores of a given genus are even greater as the number of species belonging to the given genus is higher. The comparison between benthic and pelagic species didn’t show significant differences either regarding the size of the pores, or in the distances between the pores. All species considered, the diameter of pores varies between 108 and 515 nm with a global average of 285 (± 108) nm, whereas the distance between the pores varies between 72 and 388 nm, with an overall average of 234 (± 87) nm (Fig. 8). The estimated size range of pores falls within previously reported measurements in cultured diatoms [21]. Our results show a positive relationship between the two parameters studied: the distance between pores increases with
their diameters (Fig. 9). The existing relationship permitted to calculate a distance/diameter ratio. The ratio obtained (0.85±0.26) remained fairly constant in benthic and pelagic species The constancy of the ratio remains unexplained. The comparison of the previous parameters (distance and diameter of pores) with the length, the area and the volume of the cells showed no obvious relationship (Table 1). In fact the pore size does not vary so greatly (less than 5 fold) and the pattern is maintained regardless of the cell size which varies by several orders of magnitude.
4.2 What Causes the Changes/No Changes? The contrasted environments do not seem to affect significantly the pattern of the frustule pores in either the pelagic or the benthic diatoms. We were unable to distinguish different pore pattern between the two diatom communities; no clear trend could be highlighted to explain an adaptive evolution to their respective environment. Nonetheless, in the process of natural evolution, early forms of marine diatoms (about 110 Myr ago) were pelagic and radially symmetric. It is only in the middle of the Eocene (30 Myr ago) that diatoms colonized the benthic habitats [22]. They underwent strong adaptive evolution by which diatoms with bilateral symmetry appeared. Based on our results, the basic pattern of the pores architecture may have been maintained, despite the evolutionary divergence of benthic and pelagic diatoms. 600
y = 0,79x + 106,67 R² = 0,40
500 400 Average pore diameter 300 (nm) 200 100 0
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Average distance between pores (nm)
Fig. 9 Relationship between the average pore diameter and the average distance between pores
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Additionally, we observed changes in the pore size within any given species, sometimes larger than the changes observed between species or genera. Some environmental factors, such as salinity, pH, and metal pollutants have already been shown to affect silica biomineralization and pore morphology in diatom cultures [21, 23] and [24]. In these studies, the observed alterations in response to the environmental factors are not significant (a few tens of nanometers) when compared to the variations we measured in situ. Micro- or macro-nutrient concentrations and particularly silicic acid show large seasonal variations (Fig. 5c) that may also influence the silicification processes. Diatoms living in higher silicic acid concentrations are known to be more silicified [25, 26] and have higher silica to carbon ratio [27]. Anyhow, it is difficult to discriminate between factors acting directly and the ones acting indirectly to influence the growth rate. In a case of culture diatoms, Leynaert et al. [28] have shown that under iron stress the growth rate slowed and the silicification increased. In the latter case, no qualitative analysis of the changes that may occur to the pore size was reported.
4.3 Selective Value of the Pores Architecture with Respect to Light Capture One thinks that the reasons for the ecological adaptation of diatoms in so many diverse habitats is related to their ability to exploit the differences in underwater light climate [29]. Several authors have suggested that the pores structure can improve light harvesting; thereby contributing to a better photosynthetic efficiency. Fuhrman et al. [30] have suggested that diatoms are alive “photonic crystal nanostructures” characterized by optical resonances for some wavelengths for which the propagation of light is affected. De Stefano et al. [31] have also identified a special ability of the micro-shell of the diatom Coscinodiscus wailesii in the light focusing. The frustule could partially extinguish the excessive irradiation of blue light and therefore improve the photosynthesis of the diatom [32]. These pioneer findings have been partially confirmed experimentally in the last few years by studies conducted on the diatom Coscinodiscus walesii [33, 34]. However, most of these studies have been performed on a single cleaned valve of the diatom. These experiments were usually conducted in the air, on an empty frustule, which probably modified the optical properties of the frustule compared to living diatoms living in seawater and the frustule covered with an organic layer. These experiments are however of some interest for nano-technology applications. The biological relevance of the frustule on light harvesting by living diatoms and further on photosynthesis efficiency, is currently speculative. Furthermore, most of these experimental studies were mainly conducted on
the centric diatoms: Coscinodiscus spp, having one of the largest diatom cell with centric symmetry, which may not be representative of all diatom species, with regards to the diversity of frustule patterns in nature. As above-mentioned, the role of the frustule pores in the propagation of light has already been investigated. However, none of the studies has related how the in vivo optical properties of the frustule may vary depending on the pores diameter or their distribution. In the present study, all the sizes estimated for the frustule pores are smaller than the wavelengths of light that commonly photosynthetic organisms are able to use in the process of photosynthesis (Fig. 8). When the pore diameter is below the visible wavelength range, evanescent waves are generated [30]. In this case the light no longer propagates and its intensity quickly decreases with the distance from the valve. Diatoms could take advantage of this phenomenon, particularly with their chloroplasts which are able to relocate into the cell and could tune the quantity of light they receive simply by moving closer to or farther from the diatom’s valve. But at this stage, all these phenomena remain hypothetical and have to be confirmed by future studies. Interestingly, a recent study has investigated the response to different light wavelengths on the nanostructure of Coscinodiscus granii grown in culture [12]. The authors have reported morphological changes, and particularly a decrease in pore diameter between white and green light in growth conditions, that would be sufficient to induce differences in the photonic properties of the frustule. In this context, one may think that benthic diatoms growing on the surface of sediments, receiving on average lower light intensity and only blue-green wavelengths have specificities if compared with pelagic diatoms that exploit the full light spectrum and the maximum of sunlight energy. In the present study, we found no difference between benthic and pelagic diatoms, in regard to the diameter of pores and the distance between them, despite observed differences in the intensity and the quality of light received by each community. Based on these observations, we suggest that changes in the light intensity and quality are not the primary drivers of the observed changes in the pores architecture. Taken together, results suggest that diatom species exhibit some degree of phenotypic plasticity in terms of frustule architecture; likely in response to the combination between genetically-driven processes of silica biomineralization [35] and episodic variations in environmental growth conditions which influence the chemical precipitation of silica within cells [36]. If the previous studies have provided evidences on the influence of the nanoscale features of the diatom frustules on the propagation of light, their influence on the light use efficiency in natural conditions remains unknown.
Silicon Acknowledgements We wish to thank N. Gayet and A. Jolivet for their help in SEM and image analysis, the crew of the RV “Albert Lucas” and the divers from IUEM/LEMAR for their assistance in sampling. This work was supported by the French National Research Agency (ANR Blanc - CHIVAS project) and the University of Western Brittany (UBO-BQR, IPOD project).
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