Protective Effects of Laminaria japonica Polysaccharide Composite Microcapsules on the Survival of Lactobacillus plantarum during Simulated Gastrointestinal Digestion and Heat Treatment

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Citation: Guo, H.; Zhou, Y.; Xie, Q.;

Chen, H.; Zhang, M.; Yu, L.; Yan, G.;

Chen, Y.; Lin, X.; Zhang, Y.; et al.

Protective Effects of Laminaria japonica

Polysaccharide Composite

Microcapsules on the Survival of

Lactobacillus plantarum during

Simulated Gastrointestinal Digestion

and Heat Treatment. Mar. Drugs 2024,

22, 308. https://doi.org/10.3390/

md22070308

Academic Editors: Leto-Aikaterini

Tziveleka, Efstathia Ioannou and

Vassilios Roussis

Received: 30 May 2024

Revised: 27 June 2024

Accepted: 28 June 2024

Published: 30 June 2024

Licensee MDPI, Basel, Switzerland.

This article is an open access article

distributed under the terms and

conditions of the Creative Commons

Attribution (CC BY) license (https://

creativecommons.org/licenses/by/

4.0/).

marine drugs

Article

Protective Effects of Laminaria japonica Polysaccharide

Composite Microcapsules on the Survival of Lactobacillus

plantarum during Simulated Gastrointestinal Digestion and

Heat Treatment

Honghui Guo 1,2,4,* , Yelin Zhou 1,5, Quanling Xie 1,2,4,* , Hui Chen 1,2,4 , Ming’en Zhang 1, Lei Yu 2,

Guangyu Yan 2, Yan Chen 3, Xueliang Lin 3, Yiping Zhang 1,2,4 and Zhuan Hong 1,2,4,*

Engineering Technology Innovation Center for the Development and Utilization of Marine Living Resources,

Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China;

218527212@fzu.edu.cn (Y.Z.); chenhui@tio.org.cn (H.C.); 18558969140@163.com (M.Z.);

ypzhang@tio.org.cn (Y.Z.)

2Xiamen Ocean Vocational College, Xiamen 361100, China; yulei@xmoc.edu.cn (L.Y.);

yanguangyu@xmoc.edu.cn (G.Y.)

3Haijia Flour Milling Company Limited, China Oil & Foodstuffs Corporation, Xiamen 361026, China

4Fujian Key Laboratory of Island Monitoring and Ecological Development, Island Research Center,

Ministry of Natural Resources, Pingtan 350400, China

5College of Advanced Manufacturing, Fuzhou University, Quanzhou 362200, China

*Correspondence: hhguo@tio.org.cn (H.G.); qlxie@tio.org.cn (Q.X.); zhong@tio.org.cn (Z.H.)

Abstract: To improve probiotics’ survivability during gastrointestinal digestion and heat treatment,

Lactobacillus plantarum was microencapsulated by spray-drying using Laminaria japonica polysac-

charide/sodium caseinate/gelatin (LJP/SC/GE) composites. Thermogravimetry and differential

scanning calorimetry results revealed that the denaturation of LJP/SC/GE microcapsules requires

higher thermal energy than that of SC/GE microcapsules, and the addition of LJP may improve

thermal stability. Zeta potential measurements indicated that, at low pH of the gastric ﬂuid, the

negatively charged LJP attracted the positively charged SC/GE, helping to maintain an intact mi-

crostructure without disintegration. The encapsulation efﬁciency of L. plantarum-loaded LJP/SC/GE

microcapsules reached about 93.4%, and the survival rate was 46.9% in simulated gastric ﬂuid (SGF)

for 2 h and 96.0% in simulated intestinal ﬂuid (SIF) for 2 h.

In vitro

release experiments showed that

the LJP/SC/GE microcapsules could protect the viability of L. plantarum in SGF and release probiotics

slowly in SIF. The cell survival of LJP/SC/GE microcapsules was signiﬁcantly improved during the

heat treatment compared to SC/GE microcapsules and free cells. LJP/SC/GE microcapsules can

increase the survival of L. plantarum by maintaining the lactate dehydrogenase and Na

-K

-ATPase

activity. Overall, this study demonstrates the great potential of LJP/SC/GE microcapsules to protect

and deliver probiotics in food and pharmaceutical systems.

Keywords: microcapsule; Laminaria japonica polysaccharide; gastrointestinal digestion; heat treatment;

Lactobacillus plantarum; spray-drying

1. Introduction

Probiotics are living microorganisms that have health beneﬁts for the host when

administered in adequate amounts [

]. More and more strains have been proven to be pro-

biotics and applied by humans, including Lactobacillus and Biﬁdobacterium [

]. Lactobacillus

plantarum is a lactic acid bacterium. It has many probiotic functions, such as improving the

gastrointestinal barrier function, preventing the overgrowth of pathogenic bacteria, anti-

cardiovascular-disease activity, and immune regulation [

]. Probiotics are effective when

they remain active and metabolically stable in the gastrointestinal tract and product [

Mar. Drugs 2024,22, 308. https://doi.org/10.3390/md22070308 https://www.mdpi.com/journal/marinedrugs

Mar. Drugs 2024,22, 308 2 of 16

However, L. plantarum has poor stability and is very sensitive to adverse environmental

factors such as heat, stomach acid, digestive enzymes, and bile salts [

]. Adverse environ-

ments can reduce microbial activity by destroying cell membrane integrity, reducing the

ﬂuidity and permeability of cell membranes, and inactivating crucial metabolic enzymes [

Hence, most L. plantarum has difﬁculty reaching the gut to function as a probiotic. Microen-

capsulation is considered to be an effective technique to protect probiotics from adverse

environmental conditions, ensuring that adequate amounts of probiotics enter the human

body and are released in the gut [8].

Probiotic microencapsulation consists of entrapping probiotics in a tiny particle using

natural or synthetic polymers as wall materials [

]. It can effectively prevent direct contact

between the strain and an adverse external environment, alleviate cell damage, and reduce

probiotics’ viability loss during processing, storage, and transport. In the preparation of

probiotic microcapsules, the choice of the appropriate wall material has an essential impact

on the survival rate, pH adaptation, temperature tolerance, and storage stability of the

probiotics. Moreover, the stability of the microencapsulation matrix depends upon the

strong intermolecular interactions of the materials [

]. Polysaccharides, proteins, and

lipids are commonly used as wall materials for preparing probiotic microcapsules [

Among them, sodium caseinate (SC) is a natural pH-dependent protein with an isoelectric

point of 4.6, which is biocompatible, edible, and biodegradable [

]. Gelatin (GE) is a

protein obtained from the thermal denaturation of collagen. It is one of the most important

natural polymer carrier materials. It has good emulsiﬁcation properties, ﬁlm formation,

water solubility, high stabilizing activity, and a tendency to form a ﬁne, dense network [

The combination of SC and GE can form a strong microcapsule membrane structure to

effectively protect probiotics from external damage [14].

Seaweed polysaccharide has good emulsiﬁcation, gelling, and ﬁlm-forming properties

and is an important wall material for microcapsules [

]. It can form three-dimensional

gel network structures, substrates, or protective ﬁlms, which protect and stabilize the

embedded core material. Laminaria japonica is one of the most economically important

seaweeds in China. Laminaria japonica polysaccharide (LJP) is a natural active substance

extracted from L. japonica. Its main components are alginate, fucoidan, and laminarin [

LJP has been reported to improve intestinal ﬂora disorders and obesity. It is beneﬁcial to

the human intestinal ecosystem and is considered to be a potential prebiotic [

]. The use

of LJP in the wall material of probiotic microcapsules has rarely been reported. Moreover,

the polysaccharide–protein matrix has shown great potential in delivering food-based

bioactives [

]. This work used LJP, SC, and GE as composite wall materials to construct

probiotic microcapsules. Taking L. plantarum as a representative probiotic strain, the

protective effects of the composite microcapsules on probiotics during gastrointestinal

digestion and heat treatments were evaluated. In addition, the morphology and structural

properties of the microcapsules were analyzed. This study provides a new approach to

the high-value utilization of L. japonica and the efﬁcient construction of probiotic carriers,

presenting promising applications in the ﬁelds of functional foods and pharmaceuticals.

2. Results and Discussion

2.1. Morphology and Particle Size

The SEM images of L. plantarum,L. plantarum-loaded LJP/SC/GE microcapsules, and

L. plantarum-loaded SC/GE microcapsules are presented in Figure 1.L. plantarum presents

a short, rod-like shape with a length of 1~1.5

m and a width of 0.6~0.8

m (Figure 1a).

L. plantarum-loaded LJP/SC/GE and SC/GE microcapsules exhibit a spheroidal shape

with a wrinkled surface caused by the rapid evaporation of water during spray-drying.

Compared to L. plantarum-loaded SC/GE microcapsules, L. plantarum-loaded LJP/SC/GE

microcapsules have a smoother surface, without obvious holes and cracks, and do not

easily leak bacteria. Although spray-dried microcapsules with concavities on the surface

have been shown to be smaller in size than freeze-dried microcapsules, spray-drying can

improve the mechanical strength and barrier performance of microcapsules and reduce the

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Protective Effects of Laminaria japonica Polysaccharide Composite Microcapsules on the Survival of Lactobacillus plantarum during Simulated Gastrointestinal Digestion and Heat Treatment

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