Effects of Mild Oxidative and Structural Modifications Induced by

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Functional Structure/Activity Relationships

Effects of Mild Oxidative and Structural Modifications Induced by Argon-Plasma on Physicochemical Properties of Actomyosin from King Prawn (Litopenaeus Vannamei) Flora-Glad Chizoba Ekezie, J-H Cheng, and Da-Wen Sun J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b05178 • Publication Date (Web): 19 Nov 2018 Downloaded from http://pubs.acs.org on November 22, 2018

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Journal of Agricultural and Food Chemistry

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Effects of Mild Oxidative and Structural Modifications Induced by

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Argon-Plasma on Physicochemical Properties of Actomyosin from King

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Prawn (Litopenaeus Vannamei)

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Flora-Glad Chizoba Ekezie a,b,c, Jun-Hu Cheng a,b,c, Da-Wen Sun a,b,c,d

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a School b Academy

of Contemporary Food Engineering, South China University of Technology, Guangzhou Higher Education Mega

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of Food Science and Engineering, South China University of Technology, Guangzhou 510641, China

Center, Guangzhou 510006, China c Engineering

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and Technological Research Centre of Guangdong Province on Intelligent Sensing and Process Control of Cold Chain Foods, Guangzhou Higher Education Mega Centre, Guangzhou 510006, China

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d Food

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Refrigeration and Computerized Food Technology, University College Dublin, National University of Ireland, Agriculture and Food Science Centre, Belfield, Dublin 4, Ireland

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Abstract

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In the present work, the structure and physicochemical properties of natural actomyosin (NAM)

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extracted from king prawn (Litopenaeus vannamei) and subjected to atmospheric pressure plasma jet

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(APPJ) generated in argon gas as a function of treatment time were examined. The results revealed that

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prawn NAM exhibited a correlating decrease in pH from 7.06 ± 0.03 to 6.92 ± 0.02 and slight increase

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(P > 0.05) in solubility 91.89 ± 1.57 to 96.86 ± 1.19 within the first few min of plasma exposure due to

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the formation of soluble aggregates. A rise in turbidity was also noted, confirming the occurrence of

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protein aggregation. These changes were also accompanied by a rise in emulsifying activity from 48.96

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± 1.66 to 67.31 ± 1.39 m2/g (P < 0.05) and nearly 50 % increase in foaming capacity after 5 min APPJ



Corresponding author. Tel: +353-1-7167342, Fax: +353-1-7167493, E-mail: [email protected], Website: www.ucd.ie/refrig; www.ucd.ie/sun

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exposure. The modulation of these properties occurred as a result of conformational changes in NAM

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evident by various complementary structural analyses conducted. Overall, these findings show that mild

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oxidation from argon plasma can be used for modification of protein functionality and emphasizes the

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need for optimal selection of plasma processing conditions.

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Keywords: Plasma species, actomyosin, structure, physicochemical changes, king prawn, muscle

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protein

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1.

Introduction

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Seafood items such as prawns and shrimps are highly consumed worldwide, contributing to

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approximately 16 % of global export value for fishery products. 1-3 They are widely available in the USA

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market with the prawn specie Litopenaeus vannamei also known as king prawn, one of the most popular

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species in the aquaculture industry. This specie of prawn is highly sort after not only for its rich flavor,

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moist flesh and low cholesterol level but also for its high biological value or protein content. An

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interesting subject of investigation in literature is the functionality of muscle proteins and its close

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relationship with protein structure and conformation. Protein-protein interactions such as aggregation,

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association and polymerization, are a result of changes in both secondary and tertiary structures of

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protein molecules, with implications on their physiochemical characteristics. These protein-protein

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interactions are reliant on certain factors such as temperature, pH and ionic strength.4 Natural

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actomyosin (NAM) comprising of myosin and actin is a principal component of muscle proteins. It is

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also an important criterion for judging the suitability of muscle meat processing, owing to its functional

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properties including alteration of spatial advanced structure, protein aggregation, solubility and water-

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holding capacity (WHC) and its influence on the texture of meat products.4 Additionally, an important

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characteristic of NAM complexes is its crucial role in gelation for determining the quality of fish mince 2 ACS Paragon Plus Environment


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and surimi products. To achieve adequate water holding capacity and binding properties, it is important

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to increase the elution level of myosin and actomyosin. Actomyosin is considered more soluble in high

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ionic strength (0.6 M KCl/NaCl solution) but lower salt concentration (0.05) in the intensity of bands of myosin and actin subunits between the

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untreated and different plasma-treated samples was observed in reducing conditions (Fig. 4b), which

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suggested that the plasma gas could not change the NAM molecular weight or cause breakage of the

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polypeptide chain at different time durations used in the current study. Analogously, no noticeable

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changes in actin were seen with increasing plasma exposure time. These results of electrophoretic

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patterns were also confirmed earlier.43 They reported that the number and intensity of various

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polypeptide bands of untreated and DBD-treated peanut protein samples were intact and no additional

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fragments were formed. The inclusion of DTT (dithiothreitol), which is a reducing agent used for

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disruption of S-S bonds, allows NAM proteins to assume a random coil conformation and promote

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better size separation of proteins in SDS-PAGE gels.

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On the other hand, under non-reducing conditions, the actin bands appear to be slightly affected

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as plasma treatment time progressed (Fig. 4a). This also applies to the myosin portions. These results

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suggested that the main obvious difference between results in Fig. 4a and 4b may be due to the oxidation

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in the sulfhydryl group and the subsequent formation of disulphide bonds. The remnant polymers that

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appeared at the top of the stacking gels may be due to the presence of covalent bonds, such as Tyr-Tyr,

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and active interactions of carbonyl-NH2. In general, the current results on conformational changes of

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actomyosin indicate that high energetic species provided by argon plasma may be able to dissociate

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some polypeptides present in NAM at the primary level. Though the interaction between major proteins


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may be destabilized, losses in band intensities associated with plasma species may be more apparent at

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longer treatment times or for different experimental setups.

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Effects on surface hydrophobicity and total sulfhydryl groups

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The significance of protein hydrophobicity in the structure-function relationship of various food

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proteins as affected by different treatments and/or processes cannot be overemphasized. Normally,

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protein hydrophobicity can be categorized as either aromatic or aliphatic, depending on the input of

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aliphatic and aromatic amino acid residues. In protein studies, aromatic hydrophobicity, measured by

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fluorescence, is a universally accepted biomarker used to ascertain the surface hydrophobicity of

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proteins. Hence, in the current study, the surface hydrophobicity of the king prawn NAM solution was

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determined by using ANS as the fluorescent probe. As shown in Fig. 5a, SoANS of NAM increased

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from 175.79 ± 0.4 to 273.07 ± 3.99 in the first 3 min of treatment. Between 4 and 5 min, SoANS values

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declined to 262.7207 ± 4.73 and 200.25 ± 2.16, respectively. In general, the surface hydrophobicity of

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all the treated samples was significantly higher than the control (P < 0.05). A basic justification for these

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outcomes was that structural and conformational changes in NAM during plasma exposure caused the

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hydrophobic groups to become more exposed and bound with ANS. It may also be posited that

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hydrophilic groups (protein carbonyl groups) in combination with amino acid residues were liberated to

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the surface alongside, which justified the slight increase in solubility in the first 2 min of plasma

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treatment. Perhaps some amounts of hydrophilic aggregates were formed at this point, but thereafter a

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relatively larger number of hydrophobic amino acid residues became exposed, as a result of greater

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inter/intra-molecular hydrophobic interactions, causing decline in solubility.44

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An assortment of intracellular and extracellular oxidants can convert SH groups into disulfide (S-

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S) bonds, formed within a single protein or between two different proteins, as a result of structural



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changes. SH groups are highly reactive functional groups in actomyosin.45 As shown in Fig. 5b, T-SH

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content was observed to decline as plasma treatment time progressed, especially between 2 and 5 min

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although these values were nearly at equilibrium. These observations are consistent with earlier works,

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SH content indicates the unfolding of actomyosin with time and the formation of inter- and/or intra-

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molecular disulfide bonds via SH oxidation or disulfide interchanges. However, it is important to

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mention that the near-equal values obtained in the current study indicates that although free SH contents

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tend to be released upon protein unfolding during plasma treatment, their presence may be also temporal

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as free SH groups are prone to oxidation

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molecular or inter-molecular disulfide bonds. The strong oxidizing agent can transform the thiol groups

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into disulfide bonds. Besides, reactive free radicals such as OH- , H2O

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aqueous medium to yield H2O2. The latter can oxidize liable free-SH groups to form S-S bonds, leading

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to the formation of disulphide (S-S) cross-links or even the production of sulfinic and sulfonic acids.47

where the concentration of SH groups decreased with prolonged treatment time. The decrease in T-

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i.e., they may quickly re-associate to form both intra-

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and H+ alike can react in

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Changes in intrinsic fluorescence

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Tryptophan/tyrosine (Trp/Tyr) fluorescence detection is broadly used to monitor changes in the

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tertiary structure of proteins since nonpolar amino acid residues are very sensitive to the polarity of

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proteins or their micro-environment. Several interactions including hydrophobic, electrostatic, van der

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Waals, and hydrogen bonding are involved during the formation of tertiary structure. However, among

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them, hydrophobic interactions are the key driving forces behind protein folding.48 During protein

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unfolding, hydrophobic residues at the interior of the protein structure are relocated to the protein

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surface, away from the polar environment. As shown in Fig. 6, the maximum emission wavelength of

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NAM shifted by ~3.0 nm (red shift) compared with the control after 5 min of plasma treatment. This


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indicates that the microenvironments of the amino acid residues were first altered, i.e., the exposure of

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buried Trps, and some molecular groups were then oxidized upon exposure to active species, resulting in

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the increase in intrinsic fluorescence intensity. However with continuous exposure to plasma species

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especially at 4 and 5 min of plasma treatment, the liberated Trp/Tyr residues/fluorophores and

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hydrophobic portions may have been oxidized by the active species contained in the plasma, resulting in

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the quenching of fluorescence intensity.

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Changes in secondary structures

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The main components of protein secondary structures include α-helix, β-sheet, β-turn and

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random coil. CD is a routine technique used to ascertain the secondary structure of proteins. Each

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constituent possess their distinctive CD spectra. For instance, α-helical proteins show a positive band at

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193 nm and negative bands at both 208 nm and 222 nm, while β-sheet proteins have positive bands at

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195 nm and a negative band at 218 nm.49 These secondary structures including disordered proteins can

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be affected by a variety of factors including the buffer system employed and processing conditions [78].

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The CD spectra of APPJ-treated NAMs as a function of treatment time (0, 1, 2, 3, 4 and 5 min) are

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presented in Fig. 7, indicating that untreated actomyosin had two negative bands/minima at θ209 and θ222.

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This strongly indicates the existence of mainly supercoiled α-helical structures in actomyosin recovered

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from Litopenaeus vannamei. Alpha-helix is known to be the main pattern or secondary structures in

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myosin rod and is held together by electrostatic interactions and hydrogen bonds. The CD spectra of

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NAMs exposed to argon plasma for up to 3 min were nearly comparable to control, suggesting no

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considerable changes occurred in secondary structures. However, when plasma treatment was applied

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beyond 3 min, noticeable change was observed, indicating that continuous exposure led to significant

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changes in secondary structures. By calculation using CDNN secondary structure software (Fig. 7), after



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exposure to APPJ, the proportion of different secondary structures of NAM was not significant, although

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the α-helix structure was slightly reduced after treatment for 5 min and a slight increase in other

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structures such as β-sheets and turns was noticed (Fig. 7). The current results confirm that the plasma

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density in argon gas produced during short treatment times was not sufficient to induce significant

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changes in NAM secondary structures, in particular myosin rod. However, under longer treatment

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durations, use of other gases such as air, or application of different plasma diameters, different results

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could be obtained.

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In conclusion, most seafood products are mainly composed of proteins, therefore are considered

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to be highly suitable as protein resource materials and can be used as functional ingredients in fish

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sausages and surimi‐based products. Shorter APPJ-treatment duration can positively affect the

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functional performance of NAM in such food systems. Though, it is possible that on prolonged

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exposure, higher protein oxidation and formation of hydrophobic interactions may occur. The

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information derived from this study is significant, as it provides better understanding of the fundamental

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interactions that occur which can aid the design of plasma systems with appropriate conditions that will

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achieve maximum efficiency during seafood processing. A combination of several factors including the

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plasma source, gas type, applied voltage, and substrate state ought to be considered, as this may

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influence the efficacy of CP in a process. Therefore under optimal conditions, CP can serve as a new

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tool for modification of protein properties, leading to subsequent development of new products for the

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food industry.

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Acknowledgements

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The authors are grateful to the National Key R&D Program of China (2017YFD0400404) for its

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support. This research was also supported by the Natural Science Foundation of Guangdong Province

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(2017A030310558), the S&T Project of Guangzhou (201804010469), the China Postdoctoral Science 21 ACS Paragon Plus Environment

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Foundation (2018T110873), the Agricultural Development and Rural Work of Guangdong Province

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(2017LM4173), the S&T Project of Guangdong Province (2017B020207002), the Pearl River S&T

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Nova Program of Guangzhou (201610010104), the International and Hong Kong – Macau - Taiwan

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Collaborative Innovation Platform of Guangdong Province on Intelligent Food Quality Control and

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Process Technology & Equipment (2015KGJHZ001), the Guangdong Provincial R & D Centre for the

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Modern Agricultural Industry on Non-destructive Detection and Intensive Processing of Agricultural

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Products, the Common Technical Innovation Team of Guangdong Province on Preservation and

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Logistics of Agricultural Products (2016LM2154) and the Innovation Centre of Guangdong Province for

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Modern Agricultural Science and Technology on Intelligent Sensing and Precision Control of

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Agricultural Product Qualities. In addition, Flora-Glad Chizoba Ekezie is in receipt of financial support

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from China Scholarship Council for her PhD study.

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References

494

1. Ekezie, F. G. C.; Cheng, J. H.; Sun, D.-W. Effects of atmospheric pressure plasma jet on the

495

conformation and physicochemical properties of myofibrillar proteins from king prawn

496

(Litopenaeus vannamei). Food Chem. 2019, 276, 147-156.

497

2. Dai, Q.; Cheng, J. H.; Sun, D.-W.; Zhu, Z.; Pu, H. Prediction of total volatile basic nitrogen

498

contents using wavelet features from visible/near-infrared hyperspectral images of prawn

499

(Metapenaeus ensis). Food Chem. 2016, 197, 257-265.

500

3. Dai, Q.; Cheng, J. H.; Sun, D.-W.; Pu, H.; Zeng, X. A. Xiong, Z. Potential of visible/near-infrared

501

hyperspectral imaging for rapid detection of freshness in unfrozen and frozen prawns. J. Food

502

Eng. 2015, 149, 97-104.



503

4. Zayas, J. F. Solubility of proteins. In Functionality of proteins in food. Springer, Berlin, Heidelberg. 1997, pp 6-75.

504 505

5. Liu, R.; Zhao, S. M.; Yang, H.; Li, D. D.; Xiong, S. B.; Xie, B. J. Comparative study on the stability of fish actomyosin and pork actomyosin. Meat Sci. 2011, 88, 234-240.

506 507

Page 24 of 37

6. Cheng, L.; Sun, D.-W.; Zhu, Z.; Zhang, Z. Effects of high pressure freezing (HPF) on denaturation of natural actomyosin extracted from prawn (Metapenaeus ensis). Food Chem. 2017, 229, 252-259.

508 509

7. Feng, D.; Xue, Y.; Li, Z.; Wang, Y.; Xue, C. Effects of microwave radiation and water bath heating

510

on the physicochemical properties of actomyosin from silver carp (Hypophthalmichthys molitrix)

511 530 522 519 515 529 521 514 531 523 513 534 526 532 528 524 518 516 520 512 533 525 535 527 517 536

13. 12. 11. 9. 10. 8. 8. Ko, W.-C.; Shi, H.-Z.; Chang, C.-K.; Huang, Y.-H.; Chen, Y.-A.; Hsieh, C.-W. Effect of adjustable

microstructure ]induced 20(2), ionic and H. International He, (2010). strength J.S., 89-95 whey Effects Azuma, Dairy on protein of the aofN., pressureJournal, rheology pH gel. &and Yang,

537

parallel high voltage on biochemical indicators and actomyosin Ca2+-ATPase from tilapia

538

(Orechromis niloticus). LWT - Food Sci. Technol. 2016, 69, 417-423.

539

during Setting. J. Food Proces. Preserv. 2017, 41(4), 13031.

9.

Chantarasuwan, C.; Benjakul, S.; Visessanguan, W. The effects of sodium bicarbonate on

540

conformational changes of natural actomyosin from Pacific white shrimp (Litopenaeus vannamei).

541

Food Chem. 2011, 129, 1636-1643.

542

10. Chattong, U.; Apichartsrangkoon, A. Dynamic viscoelastic characterisation of ostrich-meat yor

543

(Thai sausage) following pressure, temperature and holding time regimes. Meat Sci. 2009, 81, 426-

544

432.

545

11. Speroni, F.; Szerman, N.; Vaudagna, S. R. High hydrostatic pressure processing of beef patties:

546

Effects of pressure level and sodium tripolyphosphate and sodium chloride concentrations on

547

thermal and aggregative properties of proteins. Innov. Food Sci. Emerg. 2014, 23, 10-17


Page 25 of 37


548

12. Hsu, K.-C.; Hwang, J.-S.; Yu, C.-C.; Jao, C.-L. Changes in conformation and in sulfhydryl groups

549

of actomyosin of tilapia (Orechromis niloticus) on hydrostatic pressure treatment. Food Chem.

550

2007, 103(2), 560-564.

551

13. Yongsawatdigul, J.; Sinsuwan, S. Aggregation and conformational changes of tilapia actomyosin as affected by calcium ion during setting. Food Hydrocoll. 2007, 21(3), 359-367.

552 553

14. Inagaki, N. Plasma surface modification and plasma polymerization. CRC Press, Newyork, USA, 2014, pp 14-35

554 555

15. Mittal, M.; Siddiqui, M. R.; Tran, K.; Reddy, S. P.; Malik, A. B. Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal. 2014, 20, 1126-1167.

556 557

16. Dasan, B. G.; Onal-Ulusoy, B.; Pawlat, J.; Diatczyk, J.; Sen, Y.; Mutlu, M. A new and simple

558

approach for decontamination of food contact surfaces with gliding arc discharge atmospheric non-

559

thermal plasma. Food Bioprocess. Tech, 2016. 10, 650-661.

560

17.

Ekezie, F. G. C.; Sun, D.-W.; Cheng, J. H. A review on recent advances in cold plasma

561

technology for the food industry: Current applications and future trends. Trends Food Sci.

562

Technol. 2017, 69, 46-58.

563

18.

Butscher, D.; Zimmermann, D.; Schuppler, M.; Rudolf von Rohr, P. Plasma inactivation of

564

bacterial endospores on wheat grains and polymeric model substrates in a dielectric barrier

565

discharge. Food Control 2016, 60, 636-645.

566

19.

Ma, R.; Wang, G.; Tian, Y.; Wang, K.; Zhang, J.; Fang, J. Non-thermal plasma-activated water

567

inactivation of food-borne pathogen on fresh produce. J Hazard Mater. 2015, 300, 643-651.

568

20. Oh, Y. J.; Song, A. Y.; Min, S. C. Inhibition of Salmonella typhimurium on radish sprouts using

569

nitrogen-cold plasma. Int. J. Food Microbiol. 2017, 249, 66-71.



570

22.

Page 26 of 37

Hury, S.; Vidal, D. R.; Desor, F.; Pelletier, J.; Lagarde, T. A parametric study of the destruction

571

efficiency of Bacillus spores in low pressure oxygen‐based plasmas. Lett. Appl. Microbiol. 1998,

572

26, 417-421.

573

23.

of isolated porcine myofibrillar protein by peroxyl radicals. Meat Sci. 2014. 96, 1432-1439.

574 575

Zhou, F.; Zhao, M.; Zhao, H.; Sun, W.; Cui, C. Effects of oxidative modification on gel properties

24.

Benjakul, S.; Visessanguan, W.; Ishizaki, S.; Tanaka, M. Differences in gelation characteristics of

576

natural actomyosin from two species of bigeye snapper, Priacanthus tayenus and Priacanthus

577

macracanthus. J. Food Sci, 2001, 66(9), 1311-1318.

578

25.

NIST Atomic Spectra Database (Version 3.0) ( http://physics. nist. gov/asd3). 2005.

579 580

Ralchenko, Y.; Jou, F. C.; Kelleher, D. E.; Kramida, A.; Musgrove, A.; Reader, J.; Olsen, K. J.

26.

Wang, H.; Luo, Y.; Shen, H. Effect of frozen storage on thermal stability of sarcoplasmic protein

581

and myofibrillar protein from common carp (Cyprinus carpio) muscle. Int. J. Food Sci. Technol.

582

2013, 48, 1962-1969.

583

27.

possible mode of action. J. Agric. Food Chem. 2006, 54, 6059-6068.

584 585

28.

29.

590

Coffmann, C.; Garciaj, V. Functional properties and amino acid content of a protein isolate from mung bean flour. Int. J. Food Sci. Technol. 1977. 12, 473-484.

588 589

Pearce, K. N.; Kinsella, J. E. Emulsifying properties of proteins: evaluation of a turbidimetric technique. J. Agric. Food Chem. 1978, 26(3), 716-723.

586 587

Kong, B..; Xiong, Y. L. Antioxidant activity of zein hydrolysates in a liposome system and the

30.

Handa, A.; Gennadios, A.; Hanna, M.; Weller, C.; Kuroda, N. Physical and molecular properties of egg‐white lipid films. J. Food Sci, 1999, 64, 860-864.


Page 27 of 37

591

31.


Haskard, C. A.; Li-Chan, E. C. Y. Hydrophobicity of bovine serum albumin and ovalbumin

592

determined using uncharged (PRODAN) and anionic (ANS-) fluorescent probes. J. Agric. Food

593

Chem. 1998, 46, 2671-2677.

594

32.

protein secondary structure from circular dichroism spectra. Bioinformatics, 2002, 18, 211-212.

595 596

33.

Whitmore, L.; Wallace, B. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucl. Acid Res. 2004, 32(2), W668-W673.

597 598

Lobley, A.; Whitmore, L.; Wallace, B. DICHROWEB: an interactive website for the analysis of

34.

Surowsky, B.; Fröhling, A.; Gottschalk, N.; Schlüter, O.; Knorr, D. Impact of cold plasma on

599

Citrobacter freundii in apple juice: Inactivation kinetics and mechanisms. Int. J. Food Microbiol.

600

2014, 174, 63-71.

601

35.

2008, 41, 234016.

602 603

Gordillo-Vázquez, F. J. Air plasma kinetics under the influence of sprites. J. Phys. D Appl. Phy.

36.

Bußler, S.; Steins, V.; Ehlbeck, J.; Schlüter, O. Impact of thermal treatment versus cold

604

atmospheric plasma processing on the techno-functional protein properties from Pisum sativum

605

‘Salamanca’. J. Food Eng. 2015, 167, 166-174.

606

37.

treatment of whey protein isolate model solution. Innov. Food Sci. Emerg, 2015, 29, 247-254.

607 608

Segat, A.; Misra, N. N.; Cullen, P. J.; Innocente, N.. Atmospheric pressure cold plasma (ACP)

38.

Hrynets, Y.; Ndagijimana, M.; Betti, M. Transglutaminase-catalyzed glycosylation of natural

609

actomyosin (NAM) using glucosamine as amine donor: Functionality and gel microstructure.

610

Food Hydrocoll. 2014, 36, 26-36.

611 612

39.

Chan, J. K.; Gill, T. A.; Paulson, A. T. The dynamics of thermal denaturation of fish myosins. Int Food Res J. 1992, 25, 117-123.



613

40.

Wang, G.; Liu, M.; Cao, L.; Yongsawatdigul, J.; Xiong, S.; Liu, R. Effects of different NaCl concentrations on self-assembly of silver carp myosin. Food Biosci. 2018, 24, 1-8.

614 615

Page 28 of 37

41.

Ji, H.; Dong, S.; Han, F.; Li, Y.; Chen, G.; Li.; Chen, Y. Effects of dielectric barrier discharge

616

(DBD) cold plasma treatment on physicochemical and functional properties of peanut protein

617

Food Bioprocess. Tech. 2017, 11, 344-354.

618

42.

properties of heat-denatured ovalbumin and lysozyme. Agric Biol Chem. 1986, 50, 417-420.

619 620

Kato, A.; Fujimoto, K.; Matsudomi, N.; Kobayashi, K. Protein flexibility and functional

43.

Ji, H.; Dong, S.; Han, F.; Li, Y.; Chen, G.; Li, L.; Chen, Y. Effects of Dielectric Barrier Discharge

621

(DBD) Cold Plasma treatment on physicochemical and functional properties of peanut protein.

622

Food Bioprocess. Tech, 2017, 11, 344-354.

623

44.

Dong, S.; Wang, J.M.; Cheng, L.M.; Lu, Y.L.; Li, S.H.; Chen, Y. Behavior of zein in aqueous

624

ethanol under atmospheric pressure cold plasma treatment. J. Agric. Food Chem. 2017, 65, 7352-

625

7360.

626

45.

Kittiphattanabawon, P.; Benjakul, S.; Visessanguan, W.; Shahidi, F. Gelatin hydrolysate from

627

blacktip shark skin prepared using papaya latex enzyme: Antioxidant activity and its potential in

628

model systems. Food Chem. 2012, 135, 1118-1126.

629

46.

related modifications in complex protein mixtures. Free Radic. Biol. Med. 2006, 40, 1889-1899.

630 631

47.

634

Baldwin, Robert L. "How Hofmeister ion interactions affect protein stability." Biophys. J. 1996, 71, 2056-2063.

632 633

Eaton, P. Protein thiol oxidation in health and disease: techniques for measuring disulfides and

48.

Greenfield, N. J. Using circular dichroism spectra to estimate protein secondary structure. Nat. Protoc. 2007, 1, 2876-2890.


Page 29 of 37

635 636

49.


Satoh, Y.; Nakaya, M.; Ochiai, Y.; Watabe, S. Characterization of fast skeletal myosin from white croaker in comparison with that from walleye pollack. Fisheries Sci. 2006, 72,646-655.



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637

List of Figures

638

Fig. 1. Experimental set up of the plasma jet system, (b) typical optical emission spectra of Ar/O2

639 640 641

measured close to the nozzle outlet (at 5 mm). Fig. 2. Comparison of (a) pH and (b) turbidity at 350 nm of untreated (at 0 min) and plasma treated NAM solutions at different time intervals.

642

Fig. 3. Effects of APPJ treatment durations on (a) solubility and foaming properties, and (b)

643

emulsifying characteristics of NAM proteins. Values are the mean of n = 3 ± the standard

644

deviation. a–d Different letters indicate significant differences (P < 0.05).

645

Fig. 4. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) profiles of NAM

646

proteins from Litopenaeus vannamei subjected to APPJ treatment. (a) without DTT and (B)

647

with DTT. Lane 1: marker; lanes 2–6: samples treated for 0, 1, 2, 3, 4 and 5 min,

648

respectively. MHC = myosin heavy chain

649

Fig. 5. Effects of APPJ treatment durations on (a) surface hydrophobicity and (b) total sulfhydryls

650

characteristics of NAM proteins. Values are the mean of n = 3 ± the standard deviation.

651

Different letters indicate significant differences (p < 0.05).

652 653 654 655

Fig. 6. Changes in fluorescence spectra of NAM extracted from muscle of prawn.

a–d

a–d

Different

letters indicate significant differences (p < 0.05). Fig. 7. Changes in secondary structure of NAM subjected to APPJ treatment as measured by far-UV CD-spectroscopy.


Page 31 of 37


Ar O (777.1 nm)

Intensity (counts)

2800

O (842.3 nm)

2400 2000 1600 1200 800 400 0 200

400

600

800

1000

1200

Wavelength (nm)

Figure 1. (a) Experimental set up of the plasma jet system, (b) typical optical emission spectra of Ar/O2 measured close to the nozzle outlet (at 5 mm).



Page 32 of 37

(a)

(b) 0.5

Turbidity A350 nm

7.1

pH

7.0

6.9

0.4

0.3

6.8 0.2 6.7 0

1

2

3

4

5

Treatment time (min)

0

1

2

3

4

5


Figure 2. Comparison of (a) pH and (b) turbidity at 350 nm of untreated (at 0 min) and plasma treated NAM solutions at different time intervals.


Page 33 of 37


Solubility (%) Foaming capacity (%)

Physicochemical property (%)

100

a

a

a

a

a

b

b

60

b

c c

40

a

70

b a

80

EAI (m2/g) ESI (min)

(b)

Emuslifying propeties

(a)

60 50 40 30

a

20 20 0

c

0 1

2

3


4

5

b

d

10

0

b

bc

c

a

a

0

1 2 3 Treatment time (min)

d

4

d

5

Figure 3. Effects of APPJ treatment durations on (a) solubility and foaming properties, and (b) emulsifying characteristics of NAM proteins. Values are the mean of n = 3 ± the standard deviation. a–d Different letters indicate significant differences (P < 0.05).



Page 34 of 37

Figure 4. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) profiles of NAM proteins from Litopenaeus vannamei subjected to APPJ treatment. (a) without DTT and (B) with DTT. Lane 1: marker; lanes 2–6: samples treated for 0, 1, 2, 3, 4 and 5 min, respectively. MHC = myosin heavy chain


Page 35 of 37


(a)

300 b

So-ANS

250

a

b

c d

200

e

150 100 50 0

0

1

2

3

4

5


(b)

Total SH content (mol/g protein)

17 a

a

16 b

bc bc

c

15

14

0

1

2 3 Treatment time (min)

4

5

Figure 5. Effects of APPJ treatment durations on (a) surface hydrophobicity and (b) total sulfhydryls characteristics of NAM proteins. Values are the mean of n = 3 ± the standard deviation. a–d Different letters indicate significant differences (p < 0.05).



max value (nm), intensity

Control 1 min 2 min 3 min 4 min 5 min

Intensity

800

600

a

333.00a 333.00a 333.00b 333.00 b 335.66b 335.67

Page 36 of 37

bc

737.30 bc 742.30 c 760.01 a 805.23 b 722.47a 693.70

400

200

0 300

325

350

375

400

Wavelength (nm)

Figure 6. Changes in fluorescence spectra of NAM extracted from muscle of prawn.

a–d Different

letters indicate significant differences (p < 0.05).


Page 37 of 37


Figure 7. Changes in secondary structure of NAM subjected to APPJ treatment as measured by farUV CD-spectroscopy.


Effects of Mild Oxidative and Structural Modifications Induced by

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