Double walled carbon nanotubes promote the overproduction of extracellular protein-like polymers in Nitzschia palea: An adhesive response for an adaptive issue

Abstract

A B S T R A C TThe present study assessed the effects of double-wall carbon nanotubes (DWCNTs) dispersed in the presence of a realistic concentration of natural organic matter (NOM, 10 mg L À1 ) on the benthic diatom Nitzschia palea using toxicity tests and quantitative/qualitative extracellular polymeric substances (EPS) assays. No toxic effect was observed. A growth delay was measured after 48 h of exposure to concentrations of DWCNTs ranging from 1 mg L À1 ($29%) to 50 mg L À1 ($84%). Extracellular carbohydrates and proteins were extracted using a sequential multi-methods protocol to collect soluble, hydrophobic and ion-bridged extracellular polymeric substances (EPS). Extracted EPS were analyzed by colorimetric assays and size exclusion chromatography. The results highlighted a higher EPS concentration in exposed cultures that was primarily caused by an overproduction of protein-like polymers (protein or glycoproteins, PLPs). Such EPS overproduction and increase in proteins/carbohydrates ratio can partially explain the observed growth inhibition. EPS were preferentially extracted using hydrophobic conditions and were mainly composed of PLPs with either low (10 kDa) or high (174 kDa) molecular weights. These data highlights the affinity between DWCNTs and EPS, which is primarily driven by both physical and hydrophobic interactions. This indicates that N. palea can respond to DWCNTs by forming an EPS network optimized for adhering to and efficiently wrapping DWCNTs.

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“…Furthermore, the secretion of polysaccharides in the medium seems to be a defense mechanism of algae against heavy metals [35,72]. More recently, Verneuil et al [73] also demonstrated the role of EPS production in diatoms cultures exposed to CNTs. The authors reported the high proportion of hydrophobic proteins in EPS, which represent the primary part of extracted EPS.…”

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“…[73] On doublewalled carbon nanotubes (DWNTs), 10 and 174 kDa protein-like polymers were identified as the predominant adsorbed components of EPS secreted by Nitzschia palea. [74] In terms of the binding strength with microbial cells, the EPS from algal aggregates may be fractionated into loosely bound EPS (LB-EPS) and tightly bound EPS (TB-EPS). [75] Spectral analysis has revealed that tryptophan and humic-like components in TB-EPS exhibit higher binding capacities to CuO NPs and Fe 3 O 4 NPs than those in LB-EPS.…”

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“…These organisms are thus a critical group to look at for assessing the effects of CNPs on the environment. Effects of two different types of CNTs (double walled: DWCNTs and multiwalled: MWCNTs) were assessed on the benthic diatom Nitzschia palea [27,28]. Results showed that environmentally realistic concentrations of natural organic matter (NOM) used as a dispersant could increase the short term growth inhibition induced by CNTs.…”

“…For instance, oxidized particles appear more toxic and are associated with oxidative stress. Some characteristics, such as the presence of the cellular wall or the secretion of EPS seem to make algae more resistant [27][28][29] compared to other organisms [30]. The question of the role of oxygen-containing functions is still debated because not only this modifies the surface chemistry on the CNPs and thus their surface charge depending on the pH, but it also contributes to make them much easier to disperse in water.…”