Effect of drying on the production of fucoxanthin isomers from brown seaweeds

J Food Process Preserv. 2022;00:e17057. wileyonlinelibrary.com/journal/jfpp  

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https://doi.org/10.1111/jfpp.17057 © 2022 Wiley Periodicals LLC.

1  |  INTRODUCTION

Seaweeds can produce a variety of structurally and functionally unique bioactive components for human benefit. This is signifi- cant in a wide range of applications from the pharmaceutical to food industries (Bhuyar et al., 2021; Ramli et al., 2020). Some edible brown seaweeds have been used in major commercial in- dustries as an abundant and renewable potential source of not

only food, but also medicinal and chemical products, such as pig- ments, nutrients, cosmetics, and hydrocolloids, in Asia, partic- ularly in Japan and China (Zhu et al., 2009). Undaria pinnatifida (“wakame” in Japanese), Nemacystus decipiens (“itomozuku”), and Sargassum species have already been commercially cultivated to meet the industry's growing demand (Milledge & Harvey, 2016;

Nisizawa et al., 1987; Pan et al., 2019; Tako et al., 1999; Wang et al., 2018).

Received: 18 April 2022 

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 Revised: 27 July 2022 

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 Accepted: 15 August 2022 DOI: 10.1111/jfpp.17057

O R I G I N A L A R T I C L E

Effect of drying on the production of fucoxanthin isomers from brown seaweeds

Arif Agung Wibowo

¹

 | Philip Estera Elim

¹

 | Heriyanto

¹

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Monika Nur Utami Prihastyanti

¹

 | Jessica Renata Yoewono

²

 | Yuzo Shioi

¹

 | Leenawaty Limantara

³

 | Tatas Hardo Panintingjati Brotosudarmo

²

1Ma Chung Research Center for Photosynthetic Pigments (MRCPP) and Department of Chemistry, Universitas Ma Chung, Malang, Indonesia

2Department of Food Technology, Universitas Ciputra, Citraland CBD Boulevard, Surabaya, Indonesia

3Center for Urban Studies, Universitas Pembangunan Jaya, South Tangerang, Indonesia

Correspondence

Tatas Hardo Panintingjati Brotosudarmo, Department of Food Technology, Universitas Ciputra, Citraland CBD Boulevard, Surabaya 60219, Indonesia.

Email: tatas.brotosudarmo@ciputra.ac.id

Abstract

Fucoxanthin, an algal carotenoid with bioactivity that benefits human health, is gain- ing popularity as a functional food. Therefore, in this study, the effect of drying meth- ods and conditions on the production of fucoxanthin isomers in three closely related Sargassum species with slightly different morphological lamina were investigated. The recovery of fucoxanthin after oven- drying was 1.1– 1.3- fold higher than that after sun- drying and varied 1.6- fold among the S. species used, indicating that each algal species has a different heat susceptibility even among closely related species, and should be op- timized for each species and drying method. In Padina australis with homogeneous mor- phology, the optimal temperature to maintain all- trans form was 60°C with only a 5.3%

loss, while other cis- isomer transformations were maintained at 80°C. The apparent activation energy estimated by Arrhenius plots differed for the all- trans form and cis- isomer transformations, indicating the presence of different reactions between them.

Practical applications

Drying treatment is an efficient and cost- effective technique for reducing the mois- ture content of post- harvest seaweed to prevent decomposition, increase shelf life, and easily extract the targeted compounds. Owing to the difference in heat suscepti- bility, even in closely related species, the results indicated that it should be necessary not only to select appropriate algal species and drying methods but also to optimize the thermal conditions for each target substance of the selected material. This study provided qualitative information, particularly on seaweed drying procedures, and contributed to the production of marine products in the fields of food and bioactive substances, such as fucoxanthin isomers.

Sargassum species are naturally grown on almost all of Indonesia's coast, and in 2019, they had the highest production of brown sea- weed, reaching 1340 tons with a value of 304,000 USD for alginate purposes (BPS– Statics Indonesia, 2020). Furthermore, it is known that Sargassum species contain relatively high amounts of fucox- anthin and chlorophyll (Chl) a averaging 0.43 to 4.11 mg·g⁻¹ dry weight (d.w.) and 1.70 to 7.89 mg·g⁻¹ d.w., respectively (Heriyanto et al., 2017).

Fucoxanthin is a pigment component of brown alga that is classi- fied as a xanthophyll carotenoid possessing a distinct structure, such as allenic, epoxide, and acetyl groups. Owing to its structure, fucox- anthin is expected to provide several health benefits to humans, such as anti- obesity, anti- diabetic, anti- tumor, anti- inflammation, and antioxidant properties (Gammone & D'Orazio, 2015; Kang et al., 2014; Lee et al., 2021; Lourenço- Lopes et al., 2022; Maeda et al., 2008), and be more effective than β- carotene and lycopene in inhibiting cell growth and inducting apoptosis in human cancer cells (Hosokawa et al., 2004). The cis- isomers of carotenoids are sug- gested to enhance their incorporation into cells by increasing their solubility (Honda et al., 2017, 2018). It was demonstrated that the inhibitory effect of 13- cis and 13′- cis fucoxanthin isomers on cancer cell growth was stronger than that of the all- trans form (Nakazawa et al., 2009).

Recently, the effect of drying on the recovery of pigments and other functional compounds from various species of brown seaweed was reported (Badmus et al., 2019; Silva et al., 2019). They recog- nized the effectiveness of drying post- harvest. However, depending on the algal species and objective compounds used, the optimum temperature for drying methods involving oven, freeze, and micro- wave varied in the range of 25– 60°C. Therefore, it was concluded that the target compound of each alga must be heated to an appro- priate temperature.

In this study, we investigated the effect of drying on the recov- ery of fucoxanthin and its isomers, which have potential bioactiv- ity and health benefits for humans. Three closely related Sargassum with slightly different morphological structures were used to clarify the relationship between morphological structure and heat suscep- tibility after drying with a fixed moisture content of 10%. After dry- ing, an optimum temperature for fucoxanthin isomer production was determined in Padina australis with a simple fan- shaped structure.

The use of the intensity ratio of mass spectrometry (MS) fragment ions for the differentiation of fucoxanthin isomers with geometric fine structures is also discussed as a useful alternative method.

2  |  MATERIALS AND METHODS 2.1  |  Chemicals

Analytical grade methanol (MeOH), acetone, methyl tert- butyl ether (MTBE), and ammonium acetate were the solvents used for pigment extraction and high- performance liquid chromatography (HPLC), while liquid chromatography grade water (H₂O), MeOH, and formic

acid were used for MS analysis and were obtained from Merck (Darmstadt, Germany). Standard pigments, Chl c₁, Chl c₂, all- trans fucoxanthin, Chl a, and pheophytin (pheo) a, were obtained from NATChrom (Malang, East Java, Indonesia).

2.2  |  Seaweed samples

Three closely related but morphologically distinct S. species and P.

australis were used as algal materials. S. polycystum with large lami- nae, S. species with wide and long laminae, Sargassum filipendula with small laminae, and P. australis with fan- shaped homogenous laminae were collected from certified seaweed farms in Teluk Awur beach, Jepara, Central Java, Indonesia (6°36′46.8′′S 110°38′29.1′′E).

Photos of S. species are presented in Figure S1 (for a photo of P.

australis, refer to Heriyanto et al., 2017). The seaweed was cleaned of any associated debris by rinsing with clean seawater and then tap water. During transportation to the laboratory, samples were placed in black plastic bags and placed in a cooling box.

2.3  |  Pigment extraction

Fresh algal thalli were frozen with liquid N₂ before being ground into fine particles with a blender. To extract the pigment, 0.1 g of sample was homogenized in a vortex for 1 min with 1 ml of acetone:MeOH (3:7, v/v) and then sonicated for 1 min to break the cells. The crude pigment extract was separated from its residue by centrifugation at 10,000g for 2 min at ambient temperature. The residue was continu- ously extracted using the same procedure until the residue appeared colorless. The pigment extracts were mixed and dried in an N₂ gas stream. The dry powders from Sargassum and Padina species were extracted using a method proposed by Ishihara et al. (2008) with a slight modification. The pigments from 0.1 g of dry powder were extracted using the same methods as the fresh sample and finally dissolved in acetone.

2.4  |  Pigment determination

The pigments were identified using absorption spectrometry, HPLC, and MS analysis based on the spectral shape, maximal absorption wavelength (λ_max), and Q- ratio (spectrometry); retention time (t_R) (HPLC); and precursor and fragment ions and intensity ratio of frag- ment ions (MS). The following sections describe the specific tech- niques performed for pigment identification. The modified standard curve of the pigments from the linear equations was used to calcu- late pigment concentrations in mg·g⁻¹ d.w. (Heriyanto et al., 2017).

Similarly, fucoxanthin isomer concentrations were calculated using a linear equation based on the all- trans fucoxanthin standard curve (y = 198.89x − 335.62; R²= 0.9994, where y is the peak area de- tected at 450 nm (× 10⁻³) and x is fucoxanthin isomer concentration (μg·ml⁻¹)).

   

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2.4.1  |  Absorption spectrometry

The UV- 1700 spectrophotometer (Shimadzu, Kyoto, Japan) was used to record the absorption spectra of the pigment extracts in acetone from 300 to 800 nm. To identify the types of cis- isomers, an empiri- cal absorption ratio, Q- ratio (Aλmax cis peak/Aλmax main peak), was used.

2.4.2  |  HPLC analysis

HPLC analysis was performed using reversed- phase (RP)- HPLC with a photodiode array detector (Shimadzu). The pigment was separated using a Shim- pack VP- ODS C₁₈ column (250 × 4.6 mm i.d.) (Shimadzu), and the fucoxanthin isomers were separated using a C₃₀ column (150 × 4.6 mm i.d., 3 μm particle size) (YMC, Tokyo, Japan) according to Wibowo et al., 2022. In brief, the separation was carried out using a gradient elution program of water, MeOH, and MTBE mixture as the mobile phase at a column oven temperature of 30°C and a flow rate of 1.0 ml·min⁻¹.

2.4.3  |  MS analysis

The fucoxanthin isomers were analyzed using electrospray ioniza- tion (ESI)– LC triple quadrupole MS, LCMS- 8030 (Shimadzu), on a Chromolith Performance RP- 18e column (100 × 4.6 mm i.d.) (Merck KGaA) with an isocratic elution program of 0.1% formic acid in water (A solvent, 10%) and 0.1% formic acid in MeOH (B solvent, 90%) at a column oven temperature of 30°C and a flow rate of 1.5 ml·min⁻¹. The standard pigments were analyzed using an iso- cratic elution program of 50% A solvent and 50% B solvent with- out a column at a flow rate of 0.4 ml·min⁻¹. As previously described, MS analysis was performed in the mass range from 200 to 1000 m/z (Brotosudarmo et al., 2018). The spectral data obtained by a full Q1 scan and product– ion scan at the collision energy (CE) = −10 V from the fucoxanthin standard and its isomeric forms were saved in the LabSolution MS Library (Shimadzu) and then analyzed using the pre- viously described method (Heriyanto et al., 2021).

2.4.4  |  Fragment- ion ratio for fucoxanthin isomer identification

A novel ratio obtained from the MS analysis was used to identify the fucoxanthin isomers. Carotenoids with very similar struc- tures can be distinguished by comparing the intensities of their fragments, which are commonly the base peaks produced by the product– ion scan in the ESI– MS/MS analysis (Rivera et al., 2013;

Wibowo et al., 2022). Fucoxanthin isomers (C₄₂H₅₈O₆) had the same precursor ion at m/z 659.5 [M + H]⁺ and product ions at m/z 641.5 [M + H– H₂O]⁺ and m/z 581.4 [M + H– H₂O– HOCOCH₃]⁺ which were formed by loss of water molecule, and water and acetic acid molecules, respectively (cf. Table S2). Their ratios are defined

as follows: ratio of loss of water molecule (%) = Ifragment ion [m/z 641.5]/Ifragment ions [m/z 641.5 + 581.4] × 100 and ratio of loss of water and acetic acid molecules (%) = Ifragment ion [m/z 581.4]/Ifragment ions

[m/z 641.5 + 581.4] × 100, where Ifragment ion [m/z 641.5], Ifragment ion

[m/z 581.4]_, and Ifragment ions [m/z 641.5 + 581.4] represent the inten- sity of loss of water molecule, intensities of loss of water and acetic acid molecules, and sum of the intensities of loss of water molecule and water and acetic acid molecules, respectively.

2.5  |  Drying methods

To evaluate the efficiency of drying methods, three S. species with various lamina sizes and shapes were dried using two different meth- ods: sun- drying and oven- drying. Seaweeds (1500 g fresh weight) were oven- dried at 50°C in the dark, and sun- dried at an ambient temperature of 35– 41°C and light intensity (2060 μmol·m⁻²·s⁻¹ maxi- mum). Both drying processes were continued until the final moisture content reached 10%. P. australis was used to determine the optimal temperature for cis- isomer formation during the oven- drying treat- ment. As a sample suitable for minimizing errors between samples, P. australis has a fan- shaped homogeneous lamina and high contents of fucoxanthin (Indrawati et al., 2010). To obtain consistent dried samples, the seaweed was dried in the range 40– 100°C at 20°C in- tervals until their moisture content was 10% under dark conditions by changing the duration of drying time at each temperature as:

45.5 h at 40°C, 25.5 h at 60°C, 17.0 h at 80°C, and 5.5 h at 100°C.

This treatment reduced the weight of the samples by approximately 10%, making it easier to handle, particularly the extraction of the pigments and extension of shelf life.

2.6  |  Statistical analysis

All the experiments were carried out in triplicate with at least three samples. The average and standard error were calculated with a 95%

confidence level. Fucoxanthin isomer concentrations were calcu- lated using the same extinction coefficient as the all- trans form.

3  |  RESULTS AND DISCUSSION

3.1  |  Effect of drying on the fucoxanthin and Chl concentrations

The pigment concentrations were revealed using HPLC with a pho- todiode array detector before (fresh) and after drying treatments at 10% moisture content, as described in Section 2.5. The con- centrations of fucoxanthin in fresh seaweeds ranged from 0.88 to 0.93 mg·g⁻¹ d.w. among the three S. species, with P. australis having a 1.7- fold higher concentration (1.56 mg·g⁻¹ d.w.) than the other S. spe- cies (Table 1). These values were consistent with previously reported values of 0.75 and 1.64 mg·g⁻¹ d.w. in S. crassifolium and P. australis,

respectively (Heriyanto et al., 2017). S. filipendula with small lami- nae and long stipe had a high recovery of fucoxanthin at 97.7% and 92.0% in the oven- and sun- drying methods, respectively, whereas S. species with wide and long laminae had the lowest recovery of 62.4% and 57.0% in the oven- and sun- drying methods, respectively.

Fucoxanthin recovery after oven- drying was up to 99.9% in P. aus- tralis, while sun- drying had a low recovery of 36.0%. In terms of fu- coxanthin recovery, these results indicated that oven- drying is more effective than sun- drying. Furthermore, despite having nearly com- parable concentrations in fresh materials, their recovery by both the drying treatments varied among the Sargassum species. These dif- ferences in fucoxanthin recovery after drying appear to be primarily due to differences in the morphological structure of the lamina in the S. species. This may have resulted in different heat susceptibility. As stipe in brown seaweed has more hard tissues and high endurance to maintain pigments against heat exposure than laminae, S. filipendula had the highest fucoxanthin recovery. As opposed to fucoxanthin recovery, the sun- drying method was more effective in recovering Chl a among the three S. species, with 54% to 40.9% compared to 37.9% to 19.4% for the oven- drying method. These findings were consistent with the recovery of Chl a in P. australis after both drying treatments. Based on the findings of Badmus et al. (2019), not only the selection of algal materials but also the drying method is critical for each target material when drying treatment is used.

3.2  |  Effect of drying on the pigment composition

The absorption spectra of fresh thalli extracts, and sun- and oven- dried samples obtained from the sample algae showed nearly identi- cal absorption spectra. Qy- band decreased by 13.1– 43.1% and pheo

formation were observed in the three S. species, while its band in P. australis decreased by 18.6– 32.3%, and there was no significant absorption of pheo. In terms of fucoxanthin, as revealed by absorb- ance at 447 nm, the recovery in oven- dried samples was 50.4– 84.9%

in the three S. species and 70.6– 76.5% in P. australis, which was higher than the recovery in sun- dried samples, as shown in Table 1.

Figure S2 shows the absorption spectra of the pigments extracted from each algal species.

The pigments extracted from fresh and oven- dried seaweed were then analyzed by HPLC alongside their standard pigments to determine the pigment composition. All the brown seaweed samples were separated and identified into four main peaks. As an example, typical HPLC elution profiles of pigment extracts from S. polycys- tum are seen in Figure 1. Peak 1 corresponds to Chl c (mixture of c₁ and c₂), peak 2 corresponds to fucoxanthin, peak 3 corresponds to Chl a, and peak 4 corresponds to Pheo a, based on the t_R, λ_max, and spectral shape. Using the same identification procedures, the minor components at t_R 39 and 58 min were also determined to be Chl a' and β- carotene, respectively. Figure S3 shows the in- line absorption spectra of the peaks and standard pigments. In the fresh seaweed, at least three pigments were detected: Chl c (peak 1), fucoxanthin (peak 2), and Chl a (peak 3). According to the absorption spectrum, an additional pigment, Pheo a (t_R = 38 min), was detected in dried seaweed. Peak 2 fucoxanthin intensity varied slightly between fresh and dried seaweeds. By contrast, a significant decrease in peak 3, Chl a, was observed, indicating that a portion of Chl a was converted into Pheo a of peak 4. The MS analysis of their precursor and frag- ment ions supported the identification of the pigments from brown seaweed. Table S1 summarizes the pigment identification process.

The fucoxanthin component was then analyzed to determine its isomers using HPLC and MS analysis with pigment extracts from

TA B L E 1 Concentrations of the pigments were quantified by HPLC with a photodiode array detector before (fresh) and after drying treatments

Brown seaweed Drying treatment

Fucoxanthin Chl a

Concentration ± SE

(mg·g⁻¹) Recovery (%) Concentration ± SE

(mg·g⁻¹) Recovery (%)

Sargassum polycystum Fresh 0.89 ± 0.03 100 2.61 ± 0.18 100

Oven 0.75 ± 0.01 84.3 0.99 ± 0.07 37.9

Sun 0.58 ± 0.02 65.2 1.17 ± 0.05 44.8

Sargassum sp. Fresh 0.93 ± 0.07 100 2.47 ± 0.19 100

Oven 0.58 ± 0.02 62.4 0.64 ± 0.03 25.9

Sun 0.53 ± 0.02 57.0 1.01 ± 0.01 40.9

Sargassum filipendula Fresh 0.88 ± 0.05 100 2.37 ± 0.33 100

Oven 0.86 ± 0.07 97.7 0.46 ± 0.02 19.4

Sun 0.81 ± 0.11 92.0 1.28 ± 0.05 54.0

Padina australis Fresh 1.56 ± 0.05 100 3.81 ± 0.30 100

Oven 1.56 ± 0.11 99.9 0.80 ± 0.07 21.0

Sun 0.53 ± 0.01 36.0 0.95 ± 0.02 24.9

Note: Oven- drying treatment was performed at 50°C for 30 h in the dark, while sun- drying was performed at approximately 40°C for 36 h with light intensity of 2060 μmol·m⁻²·s⁻¹ (maximum) to reach 10% of moisture content. The results are averages of three experiments, and SE is shown.

   

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oven- dried P. australis as a sample. At least four peaks belonging to fucoxanthin isomers were well separated on a C₃₀ column within 20 min at elution times of 13.72 (peak 1), 14.88 (peak 2), 15.55 (peak 3), and 17.44 min (peak 4) (Figure S4). These fucoxanthin isomers were initially identified spectrophotometrically by comparing their

λ_max and Q- ratio (Aλmax cis peak/Aλmax main peak) from their in- line absorp- tion spectra of the HPLC (Haugan & Liaaen- Jensen, 1994), namely all- trans (peak 1; Q- ratio = 0.08), 13′- cis (peak 2; Q- ratio = 0.48), 13- cis (peak 3; Q- ratio = 0.43), and 9′- cis (peak 4; Q- ratio = 0.12) as sum- marized in Table 2. Furthermore, the purified fucoxanthin isomers from P. australis were analyzed by LCMS/MS using the modes of Q1 (+) and product ion scans (CE = −10 V) at the described analytical conditions. Table S2 shows a typical ESI– LCMS/MS spectral data.

Another newly discovered ratio through MS analysis was also used to identify the fucoxanthin isomers. As seen in Table 2, the ratio of water molecule loss (I) was highest in 13′- cis (70%) followed by all- trans (66%), 13- cis (56%), and 9′- cis (17%), while the ratio of water and acetic acid molecule loss (II) was highest in 9′- cis isomer of fucoxanthin (83%). The same results were obtained previously using high purity isomers for (I) (Wibowo et al., 2022). Therefore, either ratio, in addition to another absorption ratio, the Q- ratio, which has been frequently used to identify cis- isomers as mentioned above, is well applicable to different types of fucoxanthin isomers. Therefore, it is reasonable to conclude that this ratio is a useful alternative for identifying different types of fucoxanthin isomers, although further research into the correlation between these fragment- ion ratios and geometrical fine structures is required.

3.3  |  Effect of drying on the formation of fucoxanthin isomers

Based on the findings of the preceding study, the optimal condi- tions for fucoxanthin and its isomers were determined using the oven- drying method. Due to its simple morphological structure and to obtain homogeneous samples, P. australis was selected as the source of fucoxanthin rather than S. species. To determine the optimum concentrations of fucoxanthin isomers, oven drying tem- peratures varied from 40 to 100°C at 20°C intervals. Each sam- ple was dried to 10% of its moisture content to achieve constant drying.

As seen in Figure 2a, relatively high concentrations of all- trans fucoxanthin of 1244.1 and 1176.0 μg·g⁻¹ d.w. were obtained after 45.5 h at 40°C and 25.5 h at 60°C. This indicated that at 60°C, 94.5% of the all- trans fucoxanthin was recovered compared to 40°C F I G U R E 1 Typical HPLC elution profiles of the pigment extracts

from Sargassum polycystum detected at 430 nm (a) and the standard pigments at their λmax (b). (a): fresh (black), oven (red), and sun (green). (b): Chl c₁ (black), Chl c₂ (orange), fucoxanthin (green), Chl a (blue), and Pheo a (red).

TA B L E 2 Simultaneous separation and identification of fucoxanthin isomers by HPLC with a C₃₀ column and MS analysis

No peak t_R (min) λ_max (nm) Fucoxanthin isomer

Q- ratio Intensity

Intensity ratio (%) This study Reference^a m/z 641.5 m/z 581.4 (I)^b (II)^c

1 13.72 334, −, 451, − All- trans 0.08 0.07 8382 4350 66 34

2 14.88 333, −, 445, − 13′- cis 0.48 0.52 10,007 4346 70 30

3 15.55 332, −, 440, − 13- cis 0.43 0.45 13,886 10,678 56 44

4 17.44 332, −, 448, − 9′- cis 0.12 0.12 3435 16,215 17 83

aHaugan and Liaaen- Jensen (1994).

bIfragment ratio (I) (%) = I[m/z 641.5]/I([m/z 641.5] + [m/z 581.4]) × 100.

cIfragment ratio (II) (%) = I[m/z 581.4]/I([m/z 641.5] + [m/z 581.4]) × 100.

and nearly half the drying time. However, with increasing tempera- tures, the recovery of all- trans fucoxanthin decreased significantly, reaching 23.1% at 80°C for 17 h and nearly 10.0% at 100°C for 5.5 h of drying with the same moisture content.

Arrhenius plots are frequently used to investigate the effect of temperature on the rates of chemical reactions. This method was also used to examine the temperature- dependent results in greater detail (Figure 3). The Arrhenius plots obtained from all- trans fucoxanthin concentration measurements were biphasic with a break at 60°C, indicating the existence of two reaction processes with different straight lines (40– 60°C and 60– 100°C) for which apparent activation energies of −2.46 kJ/mol (40– 60°C) and − 58.2 kJ/mol (60– 100°C) can be calculated (Figure 3a). These negative values indicated the spontaneous degradation of all- trans isomers by heating, although, in a low- temperature phase (40–

60°C), some amounts of the isomer appear not to be degraded, but transformed to cis- isomers, since their amounts are almost equiv- alent and the low- temperature phase (40– 80°C) of cis- isomers increase with positive activation energy due to unspontaneous degradation.

In the case of cis- isomers, such as 13′- , 13- , and 9′- cis fucoxan- thin, their concentrations increased with increasing temperature up to 80°C, whereas all- trans fucoxanthin concentrations decreased (Figure 3b), indicating the occurrence of the transformation of these cis- isomers. The concentrations of all cis- isomers, including 9′- cis, increased by 16.7– 35% at 80°C and reached a maximum, then dropped sharply to those found at 40°C or less at 100°C. The Arrhenius plots obtained from the measurements of the three fu- coxanthin isomers were mostly parallel with a similar slope of lines and biphasic with a break at 80°C, switching from the formation (positive activation energy) to the degradation (negative activation energy) process. The activation energy represents the minimum amount of energy required to undergo stereomutation. The appar- ent activation energies of 13′- cis, 13- cis, and 9′- cis were calculated to be 6.44 kJ/mol (40– 80°C) and − 16.8 kJ/mol (80– 100°C), 4.12 kJ/

mol (40– 80°C) and − 12.4 kJ/mol (80– 100°C), and 4.84 kJ/mol (40–

80°C) and − 7.54 kJ/mol (80– 100°C), respectively. The Arrhenius plot was used to transform fucoxanthin isomers for the first time, and no comparable data exist. These findings imply that optimal condi- tions for fucoxanthin isomer formation differ between all- trans and F I G U R E 2 Concentrations of the fucoxanthin isomers extracted from oven- dried Padina australis at the indicated temperatures for drying time required to reach 10% moisture content. The results are averages of three experiments with SE. (a) All- trans isomer, and (b) 13′- cis, 13- cis, and 9′- cis isomers.

F I G U R E 3 Arrhenius plots of the concentrations of all- trans fucoxanthin (a) and cis- isomers of fucoxanthin (b) versus drying temperature and time for reaching 10% moisture content of the oven- dried Padina australis. The results are averages of three experiments.

   

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other cis- isomer transformations, implying the presence of different reactions between them. As demonstrated here, heat treatment im- proved the stereomutation of fucoxanthin isomers in thalli. This is the first study that reported in vivo stereomutation of fucoxanthin in algal samples by heat, although there were several reports on in vitro stereomutation in canola oil (Zhao et al., 2014) and iodine- catalyzed stereomutation in solvents (Haugan et al., 1992; He et al., 2002).

According to the findings of this study, when using drying for post- harvested dehydration, it is necessary to select and optimize the appropriate drying methods and conditions for each target ma- terial, taking into account those with different susceptibilities. Heat susceptibility varied among the three closely related S. species with slightly different morphological structures. Therefore, this study demonstrated that an appropriate temperature must be used for each target compound in each alga used (Badmus et al., 2019; Silva et al., 2019).

4  |  CONCLUSION

Drying treatment is an effective and essential technique for reduc- ing the moisture content of post- harvest seaweeds in the food and pharmaceutical industries. This study indicated that when using the drying treatment, selecting the right algal materials and drying method is crucial. This is due to differences in heat susceptibility even among closely related species. The optimal temperature to maintain all- trans form in P. australis with homogeneous morphology was 60°C with only a 5.3% loss, while other cis- isomer transforma- tions were at 80°C. The apparent activation energy estimated by Arrhenius plots differed for the all- trans form and cis- isomer trans- formations, indicating the presence of different reactions. In this study, the use of the intensity ratio of the MS fragment- ions was demonstrated to be a potential alternative method for identifying the types of fucoxanthin isomers with geometric fine structures.

Therefore, the findings of this study provided useful information on the production of fucoxanthin isomers from brown seaweed, which has health benefits for humans.

AUTHOR CONTRIBUTIONS

Arif Agung Wibowo: Investigation; Validation; Visualization;

Writing - original draft; Software; Formal analysis; Data cura- tion. Philip Estera Elim: Investigation; Formal analysis; Software.

Heriyanto: Investigation; Writing - original draft; Software; Formal analysis; Data curation; Validation. Monika Nur Utami Prihastyanti:

Validation; Writing - original draft; Formal analysis. Jessica Renata Yoewono: Writing - review & editing; Validation; Data curation.

Yuzo Shioi: Writing - original draft; Methodology; Validation;

Writing - review & editing; Supervision; Data curation; Formal analysis. Leenawaty Limantara: Funding acquisition; Writing - re- view & editing; Project administration. Tatas Hardo Panintingjati Brotosudarmo: Conceptualization; Funding acquisition; Validation;

Methodology; Writing - review & editing; Supervision; Data cura- tion; Resources; Formal analysis.

ACKNOWLEDGMENTS

We acknowledge the funding from the Ministry of Research and Technology/National Research and Innovation Agency of the Republic of Indonesia's Directorate of Research and Community Services under the Fundamental Research Scheme (grant number 005/MACHUNG/LPPM/SP2H- LIT- MULTI/AMD/VI/2020) and World Class Research (grant number 007/MACHUNG/LPPM/SP2H- LIT- MULTI/AMD/VI/2020) acquired by THPB for supporting the ex- periments, including extraction, separation/purification, analysis of carotenoids, and publication.

CONFLIC T OF INTEREST

The authors have declared no conflicts of interest for this article.

DATA AVAIL ABILIT Y STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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SUPPORTING INFORMATION

Additional supporting information can be found online in the Supporting Information section at the end of this article.

How to cite this article: Wibowo, A. A., Elim, P. E., Heriyanto , Prihastyanti, M. N. U., Yoewono, J. R., Shioi, Y., Limantara, L.,

& Brotosudarmo, T. H. P. (2022). Effect of drying on the production of fucoxanthin isomers from brown seaweeds.

Journal of Food Processing and Preservation, 00, e17057.

https://doi.org/10.1111/jfpp.17057

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The journal presents readers with the latest research, knowledge, emerging technologies, and advances in food processing and preservation. Encompassing chemical, physical, quality, and engineering properties of food materials, the Journal of Food Processing and Preservation provides a balance between fundamental chemistry and engineering principles and applicable food processing and preservation technologies. This is the only journal dedicated to publishing both fundamental and applied research relating to food processing and preservation, bene ting the research, commercial, and industrial communities. It publishes research articles directed at the safe preservation and successful consumer acceptance of unique, innovative, non-traditional international or domestic foods. In addition, the journal features important discussions of current economic and regulatory policies and their effects on the safe and quality processing and preservation of a wide array of foods.

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4/19/22, 10:21 AM Universitas Ciputra Mail - Manuscript submitted to Journal of Food Processing and Preservation

https://mail.google.com/mail/u/1/?ik=0fa1edef0e&view=pt&search=all&permthid=thread-f%3A1730505248507320777&simpl=msg-f%3A1730505… 1/1

Tatas Brotosudarmo <tatas.brotosudarmo@ciputra.ac.id>

Manuscript submitted to Journal of Food Processing and Preservation

1 message

Journal of Food Processing and Preservation <no-reply@atyponrex.com>

Tue, Apr 19, 2022 at 10:20 AM To: Tatas Brotosudarmo <tatas.brotosudarmo@ciputra.ac.id>

Dear Tatas Brotosudarmo,

Your manuscript entitled "Effect of drying on the production of fucoxanthin isomers from brown seaweeds" has been successfully submitted online and is being delivered to the Editorial Office of Journal of Food Processing and

Preservation for consideration.

You will receive a follow-up email with further instructions from our electronic editorial office platform, ScholarOne Manuscripts, typically within one business day. That message will confirm that the Editorial Office has received your submission and will provide your Manuscript ID.

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Manuscript Accepted - Updates Approved JFPP-04-22-0996.R1 [email ref: ENR-AW-1-e]

JFPP Editorial office <onbehalfof@manuscriptcentral.com> Thu, Aug 18, 2022 at 5:50 PM

Reply-To: JFPPWiley@wiley.com To: tatas.brotosudarmo@ciputra.ac.id

18-Aug-2022 Dear Dr. Brotosudarmo:

Manuscript id: JFPP-04-22-0996.R1

The final files that you submitted for your manuscript have been checked and have been found to be suitable for publication and so will be forwarded to the publisher shortly.

Sincerely,

Journal of Food Processing and Preservation Editorial Office

Tatas Brotosudarmo <tatas.brotosudarmo@ciputra.ac.id>

Journal of Food Processing and Preservation - Decision on Manuscript ID JFPP-04-22-0996.R1

Brijesh Tiwari <onbehalfof@manuscriptcentral.com> Mon, Aug 15, 2022 at 7:24 PM

Reply-To: Brijesh.Tiwari@teagasc.ie

To: 511410001@student.machung.ac.id, 511410008@student.machung.ac.id, heri.yanto@machung.ac.id, monika.nur@machung.ac.id, jessica.yoewono@ciputra.ac.id, yshioi08@gmail.com, leenawaty.limantara@upj.ac.id, tatas.brotosudarmo@ciputra.ac.id

Cc: 511410001@student.machung.ac.id, 511410008@student.machung.ac.id, heri.yanto@machung.ac.id, monika.nur@machung.ac.id, jessica.yoewono@ciputra.ac.id, yshioi08@gmail.com, leenawaty.limantara@upj.ac.id, tatas.brotosudarmo@ciputra.ac.id

15-Aug-2022 Dear Dr. Brotosudarmo:

It is a pleasure to accept your manuscript entitled "Effect of drying on the production of fucoxanthin isomers from brown seaweeds" in its current form for publication in the Journal of Food Processing and Preservation.

Your article cannot be published until the corresponding author has signed the appropriate license agreement. Within the next few days the corresponding author will receive an email from Wiley’s Author Services system which will ask them to log in and will present them with the appropriate licence for completion.

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Sincerely,

Associate Editor Comments to Author Associate Editor: Fernandes, Fabiano Comments to Author:

(There are no comments.)

Reviewer(s)' Comments to Author:

Reviewer: 2

Comments to the Author

Your revised MS is acceptable for JFPP.

Reviewer: 1

Comments to the Author

Revised version acceptable for publication.

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Fabiano Fernandes  Associate Editor  

Journal of Food Processing and Preservation

SUBMISSION ID: JFPP-04-22-0996

TITLE: “Effect of drying on the production of fucoxanthin isomers from brown seaweeds”

Dear Dr. Fabiano Fernandes,

Thank you very much for sending us the remarks of the reviewers. First, we would like to thank the referees for carefully reading the manuscript and for the helpful suggestions, to which we reply in the following way:

Reviewer #1:

1. Abstract: Well organized. Missing the novelty line?

2. Keywords: Acceptable.

3. Novelty statement: As per my opinion replace the words with, ‘we or our findings’ to ‘this study reports’.

We have changed and marked in blue. See lines, 43, 329 and 336.

3. Introduction: Need to be elaborated and improved. What are current developments in seaweed production. Following some articles relevant to the seaweed can help in the improvement of the introduction section.

https://doi.org/10.22034/GJESM.2020.01.04 https://doi.org/10.1007/s42452-021-04477-9

According to the reviewer’s comments, we have added some sentences in the Introduction and cited the references appropriately. See marked lines, 47-49.

4. Materials and methods: Acceptable. Need to be reproducible. Provide the references wherever necessary. The subsection 2.3 Data Analysis can be replaced with Statistical Analysis.

We have made the correction. See marked line of 184.

Biochemistry and Natural Product Food Technology

Tatas H.P. Brotosudarmo, Dipl.Chem.,Ph.D.

Associate Professor Universitas Ciputra CitraLand CBD Boulevard Surabaya 60219

INDONESIA

Internet:https://www.uc.ac.id/en/

e-mail: tatas.brotosudarmo@ciputra.ac.id Surabaya, 19.07.2022

5. The figure 1 can be taken in better way. Some light effects disturbing the image. High quality graphs and images need to be provided for the better understanding.

To see more clearly, we have changed the lines of Figure 1 (a) from black and white into color lines. See Figure 1 (a).

6. Results and discussion: Results well organized and explained. The discussion section missing with comprehensive comparison. I suggest authors to follow similar kinds of research for comparative assessment. Following article might help in discussion section.

https://doi.org/10.1186/s43088-019-0031-y

As far as we know, the application of fragment-ion ratio for fucoxanthin isomers and activation energy estimated for fucoxanthin transformation is our first report (https://doi.org/10.1016/j.jchromb.2022.123166) and there are no data to compare them.

We have added some sentences to explain the situations of our data. See marked lines, 255- 256 and 294-299.

7. fucoxanthin can be produced by any alternative way? If yes how this method is feasible?

There are several papers on the chemical synthesis of fucoxanthin mainly to elucidate the fucoxanthin-protein interaction. Thus, the purpose is not mass production of fucoxanthin and not considered the production time and economics. It is likely that the production from raw materials of algal is most suitable for mass production. Microalgae such as P. tricornutum have substantial fucoxanthin content. With the optimized culture parameter (McClure et al., 2018) P. tricornutum have a maximum concentration of fucoxanthin approximately 59.2 mg/g. Hence, this content could be enhanced by genetic engineering to produce a viable mutant that can produce a huge fucoxanthin amount. However, using microalgae as the source is still costly for small industries or stakeholders such as farmers. In contrast, brown algae are abundant in nature and easy to cultivate. Even though the fucoxanthin content is smaller compared to the microalgae, the economic budget efficiency is the advantage of the feasibility of the brown algae. Other than that, Iha & Fujii., 2021 successfully cultivate brown algae, which means, the production of brown algae is no longer hindered by seasonal factors.

8. Conclusion: Can be enhanced with summarized results.

We have added the summarized results. See marked lines, 318-321.

9. Units need to be standardized.

According to the comments, we have replaced Figure 3 with the new one with appropriate units.

See Figure 3.