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Volume 2 Issue 2
May  2020
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The interaction between dietary marine components and intestinal fora

  • The intestine is the natural habitat for a large and dynamic bacterial community,which perform vital metabolic and immune functions that significantly effect the nutritional and health status of the host. The major physiological functions of intestinal flora include metabolic activities that lead to important trophic effects on immune structure and function as well as protection of the colonized host against invasion by transient microbes. The intestinal flora is both a target for nutritional intervention and a factor influencing the biological activity of food compounds acquired orally. Marine environments,as a source of diverse organic compounds,can supply us with a number of beneficial and health-promoting ingredients. This review focuses on the physiological functions of intestinal flora and reciprocal interactions between intestinal flora and dietary marine components including polysaccharides,lipids,protein,taurine,carotenoids,minerals,and polyphenols. This review can serve as a valuable reference regarding the consumption of seafood and marine nutraceuticals.
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The interaction between dietary marine components and intestinal fora

    Corresponding author: Tian-Tian Zhang, zhangtiantian@ouc.edu.cn
    Corresponding author: Yu-Ming Wang, wangyuming@ouc.edu.cn
  • 1. College of Food Science and Engineering, Ocean University of China, Qingdao 266003, China
  • 2. Laboratory for Marine Drugs and Bioproducts, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

Abstract: The intestine is the natural habitat for a large and dynamic bacterial community,which perform vital metabolic and immune functions that significantly effect the nutritional and health status of the host. The major physiological functions of intestinal flora include metabolic activities that lead to important trophic effects on immune structure and function as well as protection of the colonized host against invasion by transient microbes. The intestinal flora is both a target for nutritional intervention and a factor influencing the biological activity of food compounds acquired orally. Marine environments,as a source of diverse organic compounds,can supply us with a number of beneficial and health-promoting ingredients. This review focuses on the physiological functions of intestinal flora and reciprocal interactions between intestinal flora and dietary marine components including polysaccharides,lipids,protein,taurine,carotenoids,minerals,and polyphenols. This review can serve as a valuable reference regarding the consumption of seafood and marine nutraceuticals.

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Introduction
  • A large number of microorganisms, more than 10 times the total number of body cells, are present in the human body with most located in the large intestine (Agosti et al. 2018). The intestinal tract and its flora are a dynamic diverse microbial system (Guarner and Malagelada 2003). In this system, some flora has established colonies hence maintain a symbiotic relationship with the host, while others are excreted through the digestive system. Intestinal flora use metabolites produced by the host digestive system as food, playing an important role in food digestion, such as producing vitamins and other nutrients, stimulating the immune system, resisting the invasion of foreign pathogens, and inhibiting the growth of pathogens (Sousa et al. 2017). In recent years, the differences in gut flora have drawn wide attention worldwide. Relevant research suggests that gut flora is closely related to diseases, such as obesity, immune-related diseases, and cancer (Al-Ghalith et al. 2015; Hartstra et al. 2015; Sanz et al. 2008). The difference in the gut flora among individuals not only affects the host's physiological state but also the host's psychological state, making it possible to create customized nutrition and drug treatment strategies in the management of disease (Scharlau et al. 2009; Yazigi et al. 2008).

    Human nutrition is the most important and rapid factor in terms of influencing the structure and function of intestinal flora, thereby affecting the host's metabolic status (Sela and Mills 2014). The marine environment is a source of many organic compounds that can provide humans with various beneficial and healthful ingredients (Freitas et al. 2012). Based on the findings of recently published studies, this review summarizes the reciprocal interactions between intestinal flora and dietary marine components, including polysaccharides, lipids, protein, taurine, carotenoids, minerals, polyphenols.

Physiological function of intestinal flora

    Material energy metabolism

  • The intestinal flora is involved in a variety of metabolic pathways regulating the host, including the host's immune nutrition. Importantly, the intestinal flora greatly affects the host's metabolism of dietary energy and the occurrence and development of related diseases (e.g., obesity, diabetes), playing a vital role in human metabolism (Aziz et al. 2013). Normal intestinal flora can break down food components, such as fiber and starch, and degrade polysaccharides (e.g., xylans and many plant polysaccharides). Intestinal flora can also anaerobically metabolize peptides and proteins, biotransform bile, and synthesize some vitamins (e.g., B1, B12 and vitamin K) (Cani and Delzenne 2007).

  • Antagonism

  • Probiotics can produce a variety of metabolites during reproduction in the intestine, many of which have strong inhibitory effects on pathogenic bacteria (Gaggia et al. 2010). Some enteric probiotics produce substances that have a broad spectrum of antibacterial effects. For example, substances such as bacteriocins, hydrogen peroxide, lipophilic molecules, diacetyl, carbon dioxide and acetaldehyde can exhibit bacteriostatic or bactericidal effects on Escherichia coli, Salmonella, and Streptococcus in the intestine. This ensures the dominant role of Bifidobacterium and Lactobacillus in the intestine at maintaining the stability of intestinal microflora (Marazza et al. 2013; Ouwehand 2007).

  • Barrier protection

  • Normal intestinal flora resists the invasion of pathogens by the construction of mechanical barriers, biological barriers, and immune barriers that maintain the stability of the intestinal environment as well as maintain a micro-ecological balance (Alam 2018; Camara-Lemarroy et al. 2018; Roxas and Viswanathan 2018). A biofilm-flora complex structure, such as bacterial membrane barrier, is formed by the close combination of anaerobic bacteria with intestinal mucosal epithelial cells. This combination inhibits the conglutination and colonization of intestinal and exogenous potential pathogenic bacteria on intestinal epithelial, which play an important placeholder-protection role in the intestinal epithelial tissue (Kamada et al. 2013).

  • Immunomodulatory effect

  • The intestinal flora promotes the formation of the immune system, and the immune system, in turn, can affect the formation of intestinal flora (Makita et al. 2007a, b). The presence of probiotics in the intestine can enhance specific and nonspecific immune responses and the activities of natural killer cells by activating macrophages, which enhances the expression of cytokines and immunoglobulins, especially the secretion of IgA, to improve host disease resistance (de Vrese et al. 2005). Studies have shown that Bifidobacteria in the intestine plays an important role in the formation of the immune system (Ouwehand 2007), which is reflected in the degradation of ammonium nitrite by Bifidobacteria to achieve anticancer effects. Similarly, some Lactobacillus can alter enzyme activities causing colorectal cancer in feces, such as beta-glucuronidase, azide reductase, and nitrate reductase, to achieve anticancer effects (Marazza et al. 2013).

  • Other functions

  • Intestinal flora also plays an important role in maintaining the internal stability of intestinal tissue. A recent study has shown that the intestinal flora plays a vital role in host tissue formation and homeostasis, including bone (Henning 2012). Normal intestinal flora also regulates brain development and behavior. Studies have indicated that aseptic rats exhibited changes in stress response with regulation abnormalities on hypothalamic-pituitary-adrenal axis, and weakened the pain caused by inflammation (Amaral et al. 2008).

  • Intestinal flora and dietary marine ingredients

  • A healthful diet provides sufficient nutrients to meet the basic nutritional requirements for maintenance and growth and give the body a feeling of satisfaction and well-being. Dietary components with bioactivities are susceptible to being metabolized by intestinal flora during the gastrointestinal passage prior to being absorbed (Ulluwishewa et al. 2011a, b). The metabolic activity of the intestinal flora on food ingredients can regulate the host exposure to these components and their potential health effects (Tremaroli and Bäckhed 2012) (Fig. 1). Dietary nutrition is the most important and rapid factor influencing the structure and function of intestinal flora, affecting the host's metabolic status (Laparra and Sanz 2010). Intestinal flora imbalance caused by regularly consuming an unhealthful diet plays an important role in the occurrence and development of various diseases (Barrea et al. 2018). Unhealthful eating habits can cause intestinal flora disorders, increasing intestinal permeability, forming chronic and low levels of inflammation, and further disrupting insulin signaling pathways, eventually leading to the onset of metabolic syndrome including insulin resistance, obesity, and diabetes (Avolio et al. 2020; Dong et al. 2019; Estrada and Contreras 2019; Saus et al. 2019). Many studies have shown that marine dietary components can play a significant role in maintaining and promoting human health (Dong et al. 2019). Moreover, as an environmental issue, microplastics have attracted extensive attention for their effect on health and the harm to intestinal bacteria, hence, their accumulation in the marine environment cannot be ignored (Agamuthu et al. 2019; Hantoro et al. 2019; Henry et al. 2019). This section summarizes the interaction between intestinal floras and dietary marine ingredients.

    Figure 1.  Interactions between intestinal flora and dietary components

  • Carbohydrates

  • Polysaccharides, widely distributed in animals, plants, algae, and fungi, are a class of glycans composed of more than ten monosaccharides by glycosidic bonds (Gupta et al. 2016). Straight chain linked by α-1, 4 and β-1, 4 glycosidic bonds and branch chain linked by α-1, 6 glycosidic bonds are two structural forms of polysaccharides. Compared with other sources, polysaccharides from marine foods mostly contain modification groups, such as sulfate, amido, amino, and other special structural features that exhibit unique physiological functions. Sulfated or carboxyl substituents-carrying polysaccharides with altered fermentability, such as fucoidan sulfate, galactan sulfate (e.g., carrageenan, agar) and alginate, as well as chitin modified by amino or amido (e.g., chitin, chitosan) have been the most commonly studied marine polysaccharides in recent years (Cheng et al. 2019; Ren et al. 2018; Shang et al. 2018). Some polysaccharides cannot be directly digested and absorbed by gastrointestinal enzymes, which can be transformed in the large intestine to interact with flora. The intestinal flora metabolizes carbohydrates through the glycolytic pathway, pentose phosphate pathway, and anaerobic digestion pathway (Munoz-Elias and McKinney 2006). In addition, complex carbohydrates become more simple through digestion and absorption, which can then be further fermented to short chain fatty acids (SCFA), mainly acetic acid, propionic acid and butyric acid, in the colon by intestinal flora (Morrison and Preston 2016). Given that accumulating reports have claimed that polysaccharides from marine macroalgae are a source of prebiotics, more attention has been given to marine sources as producers of important biological active substances acting on gut microbiota, especially polysaccharides from seaweed (Lindemann 2019).

    Brown algae have significant amounts of water-soluble polysaccharides named fucoidans, laminarins, and alginates. It has been reported that dietary supplements of these fermentable fiber cause changes in bacterial levels in the caecal contents of rats, with Parabacteroides distasonis detected as typical species present in rats fed with alginate and laminaran (An et al. 2013a). Alginate with high-molecular-weight, also called as alginic acid or algin, is widely used as a food additive and functional food ingredient owing to its physicochemical properties and beneficial effects on gut ecology and plays a positive role in improving human's health (Holdt and Kraan 2011). Fucoidans has a beneficial effect on gut microbiota by increasing probiotic species and increasing the concentration of total volatile fatty acids in the proximal and distal colon (Lynch et al. 2010), which has been shown to alleviate high-fat diet-induced dyslipidemia and obesity (Liu et al. 2018a, b). Duan et al. (2019) similarly demonstrated the obesity-inhibiting effect of polysaccharides from Laminaria japonica by altering the ratio of Firmicutes/Bacteroidetes. An et al. (2013b) conducted research on the effects of alginate and laminaran on rat cecal microbiota. Although the most abundant phylum in all groups was Firmicutes, Bacteroides capillosus was more abundant in the alginate group while Clostridium ramosum and Parabacteroides distasonis were the specific ones in laminaran group (An et al. 2013b).

    Carrageenans, high-molecular weight sulfated polysaccharides extracted from red algae, are generally used as additives in the food industry. Chen et al.(2018a, b) showed that polysaccharides from the red algae Grateloupia filicina (GFP) and Eucheuma spinosum (ESP) significantly promoted the growth of beneficial bacteria, such as Bifidobacteria. Gracilaria lemaneiformis (GLPs), which are both widely distributed in the marine environment, is believed to have digestion-improving and immunity-enhancing effects. Sun et al. (2018) showed that polysaccharides from GLPs had the effects on diet-induced obesity and further clarified that GLPs could repair high-fat diet-induced dysbiosis of the gut microbiota, benefiting gut health. Ren et al. (2018) studied the effect of polysaccharide extracted from Enteromorpha on cisplastin-induced small intestine injuries in mice. Their results indicated that PEP prevented cisplatin-induced alteration in fecal microbiota and repaired the damaged biological barrier. The significant intestinal repair effect was also shown by Shang et al. (2018). An interesting discovery by these investigators was that Enteromorpha clathrata polysaccharide exerted different effects on male and female microbiota.

    Not only can polysaccharides derived from marine plants regulate intestinal flora, but also those from marine animals were shown to have the same efficacy. Wang et al.(2019a, b) used DEAE Sepharose Fast Flow to obtain purified fractions of CPPS-3 from Coralline pilulifera (CPPS). Results showed that CPPS-3, containing 67.84% carbohydrate, could be broken down and used by gut microbiota, with the carbohydrate component decreasing to 30.76%. Some health-promoting gut microbiota, such as Bacteroides, Megamonas, and Veillonella were significantly enhanced, suggesting that CPPS-3 could regulate the composition of gut microbiota and be beneficial to health (Wang et al. 2019a, b). An investigation about polysaccharides derived from green-lipped mussel (GLM) showed that GLM could effectively reduce osteoarthritis symptoms with the alteration of the gut microbiota profile (Coulson et al. 2013). In addition, Zhu et al. (2018) investigated the anti-obesity effect of sulfated polysaccharide from sea cucumber (SCSP) by establishing an obesity model and interpreting the underlying mechanism, which would provide a new perspective into gut microbiota modulation of metabolic disorders. Published findings suggested that Ommastrephes bartrami polysaccharides could change the intestinal flora composition with the up-regulation of the probiotic Bifidobacterium and subsequent decrease Bacteroidetes to protect against chemotherapy-induced intestinal injury and pathogenic intestinal disorders in cyclophosphamide-treated mice (Tang et al. 2014). Shi et al. (2017) reported that dietary fucoidan from Acaudina molpadioides had a similar effect on repairing injuries induced by cyclophosphamide treatment through enriching expression of tight junction proteins and increasing the abundance of SCFA producer Coprococcus, Rikenella, and Butyricicoccus species. A study by Chen et al.(2018a, b) demonstrated that polymannuronic acid (PM) alleviated obesity and inflammation associated with consumption of a high-fat and high-sucrose diet by modulating the gut microbiome in a murine model. These results showed that PM not only decreased lipopolysaccharides in blood and ameliorated local inflammation in the colon and the epididymal adipose tissue but also had a profound impact on the microbial composition in the gut microbiome and resulted in a distinct microbiome structure, such as increased abundance of a probiotic bacterium, Lactobacillus reuteri.

    Studies have shown that oligosaccharides could also exert physiological activities beneficial to human health through interaction with intestinal flora. Zhang et al.(2017a, b) reported that neoagarotetraose (NAT), prepared using an enzyme primarily obtained from a marine microbiota to hydrolyze agar, could protect mice against intense exercise-induced fatigue damage by modulating gut microbial composition and function. Treatment with NAT for 16 days could up-regulate the anti-inflammation relating bacteria including Megasphaera and down-regulate some potential pathogens including Erysipelotrichaceae, Brevundimonas diminuta, and Coprobacillus). In addition, Zhang et al.(2017a, b) also explored the effect of NAT on gut inflammation caused by antibiotics. NAT was observed to change microbial structure accompanied by community abundance shifts in the gut microbiome. The total population increased with remarkably expanded colonization of probiotics, such as Bifidobacterium and Lactobacillus, as well as Clostridium and Prevotella, contributing to anti-inflammation and gut barrier protection. Supplementary Table S1 summarizes relevant studies that have demonstrated an impact of marine-source carbohydrates on intestinal flora in recent years.

  • Lipids

  • Lipids, a class of organic small molecules, are esters and their derivatives by the action of fatty acids and alcohols (Laguerre et al. 2015). A large proportion of lipids is digested and absorbed in the small intestine, with only 7% fatty acids able to be measured in the stool. It has been accepted that there is a very close relationship with high-fat diet-intestinal flora-obesity (Makita et al. 2007a, b). For example, the levels of Bacteroides, Bifidobacteria, and butyric acid were significantly reduced in the intestine of mice fed a high-fat diet, while Ruminal bacteria and Enterococci transform to the dominant group. Animal studies have shown that obesity is negatively correlated with Firmicutes/Bacteroides proportion, which impacts triglycerides and phosphatidylcholine metabolism by changing lipid metabolites in serum, adipose tissue, and liver, then indirectly affects energy and lipid metabolism (Ulluwishewa et al. 2011a, b).

    Notably, the biggest difference between marine lipids and terrestrial lipids is that marine lipids are rich in polyunsaturated fatty acids (PUFA) especially docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) (Cedó et al. 2015). Accumulating evidence has shown that marine lipids exhibit significant efficacy in preventing hyperlipidemia, non-alcoholic fatty acid, diabetes, cancers, inflammatory, and neurodegenerative diseases. Zhang et al. (2018) established an aging mice model induced by d-galactose to investigate the effect of tuna oil on alleviating signs and symptoms of aging. Accompanied by up-regulation of Bacteroidetes and Spirochaetes as well as the downregulation of Firmicutes, Proteobacteria, and Actinobacteria, tuna oil played a vital role in alleviating the decline of memory and cognitive levels attributed to aging.

    In addition, other studies showed such alleviation of common signs and symptoms of aging had sex-based differences in gut microbiota composition. Both sexes exhibited an increased proportion of Rikenella and decreased proportions of Macellibacteroides and Lachnospiracea incertae sedis after consumption of a dietary supplement of oil mixed with tuna oil and algae oil at a 1:2 ratio. Changes in Firmicutes, Odoribacter and Barnesiella were observed in female mice and Ruminococcus, unclassified Firmicutes, and Gemmiger in male mice, respectively (Zhang et al. 2018).

    Phospholipids (PL), a type of lipid that contains phosphoric acid, including glycerophospholipids and sphingomyelin, have received increasing attention. Phospholipids play a significant role in activating cells, maintaining metabolic functionality and balanced secretion of hormones, and enhancing the body's immunity and regeneration (Cui et al. 2017). Importantly, phospholipids also play a role in promoting fat metabolism, preventing fatty liver, lowering serum cholesterol, improving blood circulation, and preventing cardiovascular disease (Paul et al. 2019). According to differences in the head-group, glycerophospholipids are further divided into phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylserine (PS), and phosphatidylinositol (PI). Phosphatidylcholine is a choline-containing phospholipid, that primarily is in seafood, eggs, soybean, milk, red meat, and poultry. The dietary source of phosphatidylcholine is the precursor substance of trimethylamine. Its metabolites are converted into trimethylamine oxide (TMAO) by gut microbiota and flavin-containing monooxygenase-3 (FMO3), with choline and trimethylamine as the important intermediates in the process (Fig. 2). High TMAO circulation levels in vivo have been shown to be closely related to atherosclerosis, chronic heart failure, and chronic kidney disease (Gao et al. 2014). Gao et al. (2016) investigated the in vivo metabolism of TMAO following the oral gavage of different PCs, including egg yolk PC, squid PC, and soybean PC, all in the form of either emulsions or SOL on serum TMA, TMAO, choline pharmacokinetics. Results showed that time to reach peak concentration (Tmax) and production for TMA and TMAO were slower and less in the squid PC emulsion group compared with the egg yolk PC emulsion and soybean PC emulsion groups. Compared with the emulsion group, the Tmax of the choline, TMA, and TMAO in the liposome group was prolonged, and their yields were remarkably reduced. These findings indicated that squid PC could counter regulate the potential risks of TMAO production. Furthermore, PC administration in the form of liposome might eliminate TMAO production, which would provide an initial guideline about the safety of different sources of PC dietary intakes and TMAO generation (Gao et al. 2016). TMAO is commonly present in many aquatic foods. Some investigators have reported that TMAO affects microbial metabolism and intestinal microbiota (mainly Enterobacteriaceae) (Hoyles et al. 2018). Fish oil, with a high content of n-3 PUFAs, has various positive effects on human health as a commercial functional food. Our previous study suggested that dietary fish oil ameliorated TMAO-induced impaired glucose tolerance, insulin signal transduction in peripheral tissue, and adipose tissue inflammation in high-fat diet-fed mice (Gao et al. 2015). Further studies conducted by our group revealed that fish oil affected the metabolic process of the trimethylamine N-oxide precursor through trimethylamine production and FMO activity. The growth of Clostridiales was suppressed and the abundance of Bacteroidetes was increased in the fish oil-intervened group compared with the untreated C57BL/6 mice. These results indirectly implied that the low production of TMA in vivo might be attributed to the different intestinal flora resulting from the fish oil with a high content of DHA (Yu et al. 2017).

    Figure 2.  The TMAO metabolic process through intestinal flora

    A study about the effect of ω-3 long-chain polyunsaturated fatty acid (LCPUFA) on the intestinal microbiota by Wang et al. (2017) presented a detailed interpretation of the nutritive value of ω-3 LCPUFA. The results showed that the composition of gut microbiota was changed by treatment with two types of ω-3 LCPUFA. The gut microbiota enrichment in triglyceride (FO) type group decreased while in the phospholipids type group it increased. Both two types of ω-3 LCPUFA had the ability to increase the abundance of Lactobacillus animali, Lactobacillus animalis, Akkermansia muciniphila, Ruminococcus, and Lactococcus lactis, bacterial species that included probiotic strains. Interestingly, phospholipids type ω-3 LCPUFA had greater superiority for human health than did triglyceride type ω-3 LCPUFA. This might be attributed to Streptococcus thermophilus in the PL group being inferior to the FO group, hence improving anti-inflammatory properties (Wang et al. 2017).

    DHA/EPA enriched phospholipids are ubiquitous ingredients with various bioactivities in marine foods. However, there is a lack of relevant studies about the interaction of DHA/EPA-enriched phospholipids on intestinal microbiota. The impacts of DHA/EPA-enriched phospholipids and the comparison of PL species on intestinal flora should be discussed in future works.

  • Protein, polypeptides, and amino acids

  • About 12-18 g protein of human daily intake (about 10%) can enter the large intestine, including residues of dietary proteins and enzymes secreted by the small intestine. Protein-degrading bacteria living in the intestinal tract are mainly Bacteroides, Fusobacterium, Fusobacterium, and Streptococcus. Protein can provide nutrients, such as carbon, nitrogen and sulfur for bacteria after degradation.

    Marine life, including fish and shellfish, is rich in protein and essential amino acids (Shahidi and Ambigaipalan 2015). In particular, the lysine content in seafood is much higher than that of plant foods and is easily absorbed by the body. It has been reported that dietary proteins from different sources including fish could rapidly alter the microbial composition in rat caecum as quickly as two days (Zhao et al. 2017). Protein from seafood led to less energy intake and weight gain than that from meat as well as altered the gut microbiota (Holm et al. 2016). Administration of a Western diet (WD) containing lean seafood (seafood WD) for 12 weeks could reduce fat mass compared with a WD containing lean meat (meat WD) (Wu et al. 2011). Significant differences in the relative abundance of operational taxonomic units (OTUs) were reported between these two WDs-treated groups. The seafood WD group exhibited a high relative abundance of one OTU from the genus Robinsoniella, while the meat WD group possessed a high relative abundance of two OTUs from the genus Bacteroides, which might have been influenced by dietary protein source (Wu et al. 2011). It is noteworthy to report that the white meat protein (including fish) group showed a higher abundance of Lactobacillus, which has commonly been considered to play a critical role in host metabolism and inflammation-alleviation activity.

    In addition to generating SCFAs, H2, and CO2, other substances including ammonia, phenols, indoles, amines, and H2S are produced by deamination and decarboxylation after the microbial degradation of food proteins and endogenous proteins that have not been digested and absorbed by the small intestine (Geypens et al. 1997). These metabolites impact the health of the body. For example, tyrosine and phenylalanine are metabolized by intestinal anaerobic bacteria to generate phenol, p-toluene, and phenylacetic acid at the terminal end of the colon (Macfarlane and Macfarlane 1997). Sulfur-containing amino acids, such as cysteine and methionine, generate sulfides under the action of E. coli, Salmonella, Clostridium and Enterobacter aerogenes (Iarashi and Kashiwagi 2010). Aliphatic amino acids including arginine, ornithine, and methionine, could produce polyamine compounds, such as spermine, spermidine, putrescine, cadaverine, under the action of Enterobacter, Lactobacillus, Bifidobacterium and Clostridium (Tiihonen et al. 2010). These polyamines could be combined with a variety of macromolecular substances in colonic cells, which further affect the growth and reproduction of cells, thereby inducing diseases. Valine, leucine, and isoleucine could produce branched-chain fatty acids, isobutyric acid, 2-methylbutyric acid, and isovaleric acid, respectively (Allison 1978). Increased production of these substances can disrupt the intestinal flora balance and cause inflammatory bowel disease or obesity. Meanwhile, protein is also the main source of l-carnitine, which could produce trimethylamine causing atherosclerosis during the fermentation process (Wang et al. 2019a, b).

    It is generally believed that H2S is a toxic product that can induce DNA damage in the body, cause genetic changes in colon cells, and lead to intestinal diseases, such as colon cancer (Carbonero et al. 2012). Notably, Carbonero et al. (2012) reported that the inhibition of H2S synthesis in healthy mice caused damage to the small intestine and colon mucosa as well as triggered an inflammatory response, which could effectively be alleviated by supplementation with H2S. Russell et al. (2013) found that some colonic dominant bacteria utilized three aromatic amino acids. The content of benzene derivatives in feces, which have anti-inflammatory and antibacterial activities, increased as the protein intake increased. These data suggest that although protein metabolites have some toxicity, they are essential to homeostasis and health. Additionally, the difference in protein metabolism products might be related to the regulation of nitrogen balance after intestinal flora fermented the ingredients of whole-grain cereals, suggesting the intestinal flora's digestion of protein and dietary nutrients, such as high fiber diet, might influence each other (Ross et al. 2013). However, there is a lack of research studying the impact of marine-derived proteins on intestinal flora, suggesting the need for future work.

    Taurine, also called β-aminoethanesulfonic acid, is a free amino acid present in abundance in seafood (Sasaki et al. 2017). Numerous studies have showed that taurine exhibits various functions including antioxidation, regulation of cholesterol metabolism and glucose homeostasis, anti-obesity effect, promotion of hepatic metabolism and alleviation of cadmium toxicity (Rodrigues et al. 2016). Yu et al. (2016) studied the effect of taurine on gut microbiota in mice and the results showed that taurine could significantly reduce the pathogenic bacteria Proteobacteria (especially Helicobacter) abundance accompanied by an increase in Bacteroidia and Bacilli. However, another study reported that taurine could not change the human colonic flora composition and its metabolism using a human fecal single-batch fermentation system, suggesting taurine might directly act on the large intestine to exhibit anti-inflammatory activity rather than depending on the intestinal flora (Sasaki et al. 2017).

Others

    Phytochemicals

  • Carotenoids are a family of large molecular weight organic compounds consisting purely of hydrocarbons without oxygen (Gammone and D'Orazio 2015). Astaxanthin is one of the major carotenoids in marine organisms, which is commonly found in shrimp, crabs, fish, and algae (Liu et al. 2018a, b). Accumulating evidence has confirmed that astaxanthin could serve as a functional nutrient through regulation of intestinal flora. Liu et al.(2018a, b) indicated that astaxanthin effectively relieved inflammation in mice fed with a high-fat liquid diet containing alcohol. Astaxanthin significantly decreased Bacteroides in severe alcoholic hepatitis mice and Proteobacteria associated with imbalanced microecology-induced disease, as well the genera Butyricimonas and Bilophila. It remarkably increased probiotic bacteria such as Akkermansia, suggesting a critical role in improving the gut barrier (Liu et al. 2018a, b ; Wu et al. 2017).

    Phenolic compounds, a class of substances that contain phenolic hydroxyl groups in their molecular structure, are divided into monophenols and polyphenols based on the number of phenolic hydroxyl groups (Ross et al. 2013). Most seaweed halogenated phenols are brominated monophenols and their derivatives as well as brominated diphenol compounds (Wang et al. 2018). Easy oxidization and polymerization has resulted in the formation of complex polyphenols in algae (Hifney et al. 2016). Intestinal flora could promote the metabolic degradation of polyphenols, which could relieve hyperlipidemia and regulate lipid metabolism with modulation of intestinal flora (Sirk et al. 2011). A large volume of evidence has shown that marine algae contain a variety of biologically active phenolic compounds. Green macroalgae Enteromorpha Prolifera polyphenols (EPE3k) mitigated the effects of a high-fat/high-sucrose diet and streptozocin-induced diabetes in mice (Lin et al. 2019). In the same study, these investigators also showed green macroalgae significantly increased the relative abundance of Akkermansia and decreased the proportion of Alistipes and Turicibacter. Zhao et al. (2018) reported the anti-diabetic activity of Lessonia nigrescens ethanolic extract. Specifically, Lessonia nigrescens ethanolic extract could selectively enrich the amounts of beneficial bacteria, Barnesiella, as well as reduce the abundances of Clostridium and Alistipes.

  • Minerals

  • The minerals in food have special biological activity and exert certain effects on the composition of the host gut flora. Marine organisms are rich in minerals. The organic acids produced by intestinal flora during fermentation can promote the combination of minerals and amino acids hence increasing their absorption rate. A magnesium-rich marine mineral blend (MMB) was found to significantly enhance the diversity of gastrointestinal microbiota, such as health-maintaining bacteria Ruminococcaceae, Christensenellaceae, and Porphyromonadaceae, which all exhibit a protective effect on gut health after antibiotic treatment (Crowley et al. 2018). Moreover, multimineral natural products obtained from the skeletal remains of the red marine algae, Lithothamnion calcareum, (also known as Phymatolithon calcareum), have been reported to protect mice from high-fat diet-induced polyps, hyperplasia in the colonic mucosa, and inflammatory foci throughout the gastrointestinal tract (Aslam et al. 2012).

  • Problems and prospect

  • It is clear that marine environments, as a source of diverse organic compounds, can supply us with a number of beneficial and health-promoting ingredients. Consequently, the consumption and utilization of seafood have been increasing in recent decades with the continuous advancement of research on marine living resources.

    However, in spite of knowledge obtained from animal experiments, studies on humans should be conducted focusing on the changes in intestinal flora structure and related metabolites to determine the relationship among dietary marine components, intestinal flora, disease prevention and their mechanism. In addition, most studies of intestinal microflora usually neglect examining the effect of the flora on nutrient uptake in the small intestine. The bioactivity and health effects of metabolites produced by dietary marine constituents under the action of the intestinal microflora needs to be studied to identify beneficial constituents that can be used in disease prevention as a component of drugs, and as a healthful food source.

    It has been accepted that gut microbiota can explain the effects of dietary marine constituents on host physiological functions. The interaction of these constituents with intestinal microflora is of great importance in sustaining human health.

Acknowledgements
  • This work was supported by National Key R&D Program of China (2018YFD0901103), National Natural Science Foundation of China (31901688), National Natural Science Foundation of China-Shandong Joint Fund for Marine Science Research Centers (U1606403), Natural Science Youth Foundation of Shandong Province (ZR2019QC004), Laboratory for Marine Drugs and Bioproducts of Pilot National Laboratory for Marine Science and Technology (Qingdao, LMDBKF20 1807).

Author contributions
  • Lin Li wrote the manuscript. Tiantian Zhang and Changhu Xue revised the manuscript. Tiantian Zhang and Yuming Wang developed the concept and designed the outline.

Compliance with ethical standards

    Conflict of interest

  • The authors declare they have no confict of interest.

  • Human and animal rights statement

  • This article does not contain any studies involving human subjects or animals performed by any of the authors.

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