Abstract
Macroalgae play a crucial role in marine ecosystems when they contribute to the global primary production in the habitats formation, providing food and shelter to a range of aquatic organisms. They have a number of interactions with bacteria and other organisms such as fouling and disease. To inhibit the settling, growing, and biofilm formation by bacteria, it has been suggested that the macroalgae influence bacterial metabolism and quorum sensing through the production of secondary metabolites with antibiotic effect. Macroalgae-bacteria interactions have been investigated for many years. These interactions can be beneficial when the bacteria assist with the normal development of macroalgae as well as reducing secondary fouling on the algal surface. On the other hand, the interactions may have a deleterious effect when the biofilm impairs the photosynthetic ability or promotes disease development. This review reports the recent advances in the understanding of bacteria-brown algae interactions, highlighting the diversity and functional role of epiphytic bacteria, including the maintenance of the health of the algae and the biological activities described from this association. Through combined bacterial culture, microscopy, and molecular biology, it has been possible to identify and establish the phylogenetic origin of different bacterial communities associated with brown algae, being predominantly the phyla Proteobacteria, Bacteroidetes, and Firmicutes. Further investigation of the bacterial communities that live on different macroalgae using new technologies are still required, mainly to evaluate the production and secretions of metabolites with biotechnological potential.
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Introduction
Marine macroalgae are eukaryotic, photosynthetic, sessile (usually), and multicellular organisms. They are one of the main producers at the aquatic ecosystem and they contribute to almost half of the aquatic global production (Graham and Wilcox 1999). Moreover, they serve as housing to many epibiont species and they also provide suitable substrata for microorganism attachment as well as producing many organic substances that function as nutrients for bacterial multiplication and bacterial biofilm production (Singh et al. 2013).
Bacteria associated with marine algae play an important role, directly or indirectly, in normal algal morphological development, on their growth, defense against fouling organisms, and metabolism (Goecke et al. 2010). It should be highlighted that the behavior of the macroalgae in ecological and industrial (pharmacological) environments cannot be understood without considering the interactions with the associated microbiota (Egan et al. 2013). Many studies have proposed that there is a mutualistic relationship in which the bacterial community protects the host algae against secondary biological fouling, while the host surface provides nutrients and physical protection to the associated bacteria (Penesyan et al. 2010).
Despite countless examples reporting advantages in algae-bacteria relationships, this interaction is not always beneficial, because once the bacterial communities compromise the algal tissue and algal photosynthetic capability (Hollants et al. 2013), they can induce new diseases as well as pathogens that can compromise the health of the host algae (Zozaya-Valdes et al. 2015). These observations have led to investigations of the potential of extracts and/or isolated products from different marine sources, particularly from algae, against numerous organisms, including viruses and bacteria, as possible pharmaceuticals. Furthermore, the bacteria associated with algae also represent an important potential source of new promising substances, as new bioactives and antimicrobial metabolites (Egan et al. 2008; Penesyan et al. 2009; Ismail et al. 2016).
In the last decades, a great effort has been directed to the study of bacterial communities associated with algae aiming to understand the structure, succession, and dynamics of these communities in relation to ecology starting on the bacteria-algae interaction (Table 1). Most information related to algae-bacteria interactions is from studies involving green and red algae as a model for physiological and/or ecological studies (Tapia et al. 2016). These studies have demonstrated that the specific bacteria presence is necessary for morphological development and growth in green (Singh et al. 2011a; Spoerner et al. 2012; Wichard 2015; Grueneberg et al. 2016; Ghaderiardakani et al. 2017), red (Singh et al. 2011b; Fukui et al. 2014), and brown algae (Tapia et al. 2016). Bacteria are also known to induce zoospore colonization (Singh et al. 2013; Vesty et al. 2015) and spore release (Weinberger et al. 2007; Singh et al. 2015; Tapia et al. 2016). Furthermore, bacteria associated with benthic algae have ecological roles such as establishment of planktonic propagules (larvae, spores, bacteria) (Steinberg and de Nys 2002; Othmani et al. 2016; Satheesh et al. 2016) and host defense against deleterious microorganisms (Goecke et al. 2010; Singh and Reddy 2014; Campbell et al. 2015).
The identification of bacteria that inhabit macroalgae has been the object of multidisciplinary studies involving taxonomy and ecology. These have identified the phyla Proteobacteria and Firmicutes as the most abundant on macroalgal surfaces as reviewed by Hollants et al. (2013). This multidisciplinary approach is more common in research on biofilms on marine algae, where combined tools from bacteria culture, microscopy, and advanced molecular biology are used to characterize bacteria communities and explore many questions related to occurrence, distribution, persistence, and physiological and ecological functions of associated bacteria (see reviews by Steinberg et al. 2002 and Goecke et al. 2010). There is extensive literature on larvae induction and inhibition, marine algae pathogenesis, bacterial signaling molecular biology, macroalgal allelopathic chemical defenses, focusing on the general chemical structure of the colonization surface (Friedrich et al. 2001; Egan et al. 2013; Hollants et al. 2013). However, detailed knowledge of algal interaction with associated microorganisms on algae surfaces needs better understanding (Steinberg et al. 1998; Steinberg and de Nys 2002; Kubanek et al. 2003).
Brown algae (Phaeophyceae) have important ecological roles on costal ecosystems and they are one of the most diversified groups of benthic algae (Andersen 2004; Cock et al. 2011), and therefore it is of particular interest to specifically focus on the ecological roles of bacterial communities associated with these algae. Bacteria have been described in association with brown algae (Hengst et al. 2010; Lachnit et al. 2011), and some initial observations exist which connect the bacterial presence to development and growth (Pedersén 1968). To elucidate the basic aspects of brown algal biology, small filamentous species such as Ectocarpus siliculosus have been chosen as study models (Peters et al. 2004; Tapia et al. 2016). Lobophora species also have been used to investigate associated bacteria and potential induction on coral bleaching (Vieira et al. 2016).
Therefore, the aim of this review is to provide new information about (1) the diversity of bacteria associated with brown algae communities; (2) the role of biofilm on the brown algae surface; and (3) the exploration of secondary metabolite production, beginning with bacteria-brown algae interactions to discover new biological activities. To accomplish this, a literature review on the interaction of brown algae-bacteria was carried out between the years 2010 and 2018. In this search, the online databases used were Scifinder, Science direct, and Pubmed, with following keywords: “bacteria-brown algae interaction,” “biofilm and brown algae,” “biological activity and brown algae,” “algae and bacteria,” “EPS and algae,” “bacterial communities and seaweeds,” “isolation of bacteria and seaweed.” The evaluated studies were selected according to the information on the isolation and identification of bacterial communities on the surface of brown algae and on the types of interactions between brown algae and bacteria, as well as the biological activities already tested using brown seaweeds and/or bacteria. Studies addressing the isolation and identification of bacterial communities taken from water or marine sediments and work involving the transformation of heavy metals by bacteria or the association of bacteria and microalgae were excluded.
Bacterial communities associated with brown algae
Marine macroorganisms live in persistent contact with diverse microorganisms that are abundant and ubiquitous in the surrounding seawater and with biofilms on their surfaces (Wahl et al. 2012). Brown algae represent an important component of the infralittoral zone, which is present in temperate, tropical, and subtropical ecosystems (La Barre et al. 2010). Brown algae have a greater structural complexity when compared to other benthic algae. They produce chlorophyll a and c, and the carotenoids such as fucoxanthin as the most abundant photosynthetic pigments (Teixeira 2013). Macroscopic marine organisms live in persistent contact with many microorganisms that are abundant and omnipresent in the surrounding seawater (Wahl et al. 2012; Kouzuma and Watanabe 2015). Therefore, the marine algal surface provides a suitable substrate for microorganism attachment and they produce many organic substances that function as nutrients for bacterial replication and biofilm formation (Lachnit et al. 2013).
Microbial communities that live on the surface of algae are highly complex, dynamic, and consist of consortia of microorganisms, including bacteria, fungi, diatoms, protozoa, algal spores, and marine invertebrate larvae (Burke et al. 2011a; Satheesh et al. 2016). Although there is a strong pressure on the colonization by epibiont bacteria, many marine algae host microbial communities on their surfaces that differ both in quality and in quantity from the free-living bacteria in their surrounding environment (Lachnit et al. 2013).
One of the critical points involving bacterial communities is the limitation of identification techniques. Recent advances in sequencing technology have enabled researchers to characterize microbial diversity at previously unattainable scales such as the Human Microbiome Project (HMP 2012). Given the lack of a commonly accepted bacterial species concept, a phenomenological approach to categorizing microbial diversity is often chosen in practice—operational taxonomic units (OTU), defined as clusters of 16S/18S small subunit (SSU) rRNA gene similarity are used (Bondoso et al. 2013; Schmidt et al. 2014). Bondoso et al. (2013) applied denaturing gradient gel electrophoresis (DGGE) with 16S rRNA gene-specific primers for Planctomycetes to compare the communities of these organisms developing on various macroalgae. Shannon diversity indexes showed that DGGE profiles were similar in all the macroalgae. Ismail et al. (2016) studied antibacterial activities of epiphytic bacteria isolated from brown alga Padina pavonica based on 16S rRNA gene sequences. The antimicrobial activity was assessed as inhibition of growth of 12 species of pathogenic bacteria.
Epiphytic marine bacteria are intimately associated with brown algae. Between 2010 and 2018, 35 articles reported the presence of bacteria in 46 species of brown algae (Fig. 1). Among the most abundant bacterial communities are the phyla Proteobacteria, Bacteroidetes, and Firmicutes (Singh and Reddy 2014). It is suggested that the predominance of these bacteria is related to their capability to resist the effects of many stress parameters in addition to having high efficiency production system (Cray et al. 2013). Only a few studies dedicated to comprehensive assessments of total bacteria communities on algal surfaces, especially brown algae exist. However, beginning with data based on genetic sequencing, it has been revealed that the bacterial communities associated with algae are different from the planktonic bacterial communities (Burke et al. 2011b; Goecke et al. 2013). Marine macroalgae typically host diverse bacterial groups with density that varies from 102 to 107 cells cm−2, depending on the macroalgal species, thallus section, and season (Tujula et al. 2006; Bengtsson et al. 2010; Egan et al. 2013). Previous studies have reported that algae occurring in the same ecological niche have a specific bacterial community for each algae species. In contrast, macroalgae, which belong to the same species, but which occur in a different geographic location, have similar bacterial communities (Nylund et al. 2010). The specificity of bacterial communities with macroalgae may be related to three possible processes: (a) algal propagules can take specific biofilm to other areas, (b) algal chemical defenses may selectively inhibit the growth of other biofilms than that specific for host algae, and (c) algal attractants may facilitate the colonization of certain bacterial strains (Lachnit et al. 2009).
The bacterial communities associated with algae not only vary from species to species but also show temporal variation (Lachnit et al. 2011). These authors studied the epibacterial community associated with the benthic alga Fucus vesiculosus at different sampling times. They observed that among the algal bacterial community, 7–16% of sequences belonged to specific species on the host alga. For example, for F. vesiculosus, the closely related strains (Octadecabacter arcticus-Alphaproteobacteria; Granulosicoccus antarcticus-Gammaproteobacteria; Bacteroidetes-Bacteroidetes; Roseibacillus spp.-Verrucomicrobia; Planctomyces sp.-Planctomycetes) represented 16.21% of similarity between specific bacteria. In addition, other factors such as season and life cycle of the host algae can affect the associated bacterial community composition (Singh et al. 2013). Staufenberger et al. (2008) studied bacteria communities associated with the rhizoids, cauloid, meristem, and phylloid of the brown alga Laminaria saccharina (= Saccharina latíssima). They observed that the association obtained from cauloid and meristem were more specific, while the less specific associations were obtained from the more aged phylloid. Seasonal and geographic differences in the associated communities were also observed.
Clearly, there are many explanations for the host algae specificity and the temporal variations of the bacterial community associated with these algae (Singh and Reddy 2014). Epibacterial communities are sheltered in different ways (temporal and spatial on thallus distribution) on the algal surface due to biochemical and metabolite composition (Cray et al. 2013). For example, the fucoidan-degrading activity of Verrucomicrobia, members of Flavobacteriaceae and Gammaproteobacteria, suggest selective colonization on Fucus (Barbeyron et al. 2008). However, Lachnit et al. (2013) observed that F. vesiculosus carried on its surface a specific bacterial community that belongs to the phylum Proteobacteria and Bacteroidetes.
Studies focused on brown algae indicate that these bacterial communities also can act, directly or indirectly, on the morphology and reproduction (e.g., Ectocarpus sp.; Tapia et al. 2016) and on the settlement inhibition of marine biofilm bacteria and barnacle larvae (Othmani et al. 2016).
Bacterial biofilms
Biofilms are complex associations of microorganisms, immobilized on surfaces and incorporated in an extracellular biological matrix which consists of extracellular polymeric substances (EPS) secreted by cells (Silva et al. 2011). As highly complex communities in natural environments, they are characterized by the interaction with a complex of biotic communities, by genetic diversity, structural heterogeneity, and the EPS itself (Joint et al. 2007; Grossart 2010). They can grow in a high variety of surfaces, including live tissues, medical devices, industrial or potable water system pipes, and natural aquatic systems (Donlan 2002). In marine ecosystems, two bacterial populations usually exist: the planktonic, which exist freely in the water column and the sessile, as a unity bonded to a surface or at the limits of a biofilm (Egan et al. 2013).
Biofilm growth is governed by a series of biological, physical, and chemical processes, being denominated by the adherence of the binding between a cell and a substrate and cohesion, the binding between cells (Fig. 2). These mechanisms are behind the fixation forms that determine the adhesive and cohesion properties that a biofilm will exhibit (Garrett et al. 2008).
Among the stages of biofilm formation, at first a planktonic bacterium will interact with organic and inorganic compounds on a surface and form an initial and temporary structure. This first attachment is deemed reversible. However, with time, the attachment becomes more strongly connected to a surface and subsequently, irreversible (Kostakioti et al. 2013). Secondly, the bacteria which first colonized the substrate accumulate in the biofilm through growth and reproduction, thus changing the surface composition creating a suitable environment for colonization by other bacteria. Thirdly, planktonic bacteria and those that are bonded to each other communicate by quorum sensing (QS). This communication mechanism plays a vital role on gene expression synchronization inside the bacterial community (Garrett et al. 2008; Kostakioti et al. 2013). Therefore, bacterial biofilm forming communities provide a favorable substrate for the attachment of different microorganisms; the organic and inorganic contents of EPS provide nutrients to phytoplankton and macroalgae for their survival (Mandal et al. 2011; Singh et al. 2011c).
EPS is a matrix composed of polymeric substances, especially exopolysaccharides (40–95%) and proteins (60%), as well as nucleic acids (10%) and lipids (40%) (Flemming and Wingender 2010). These substances protect the bacterial cells from the external environment and facilitate their communication through chemical and physical signals, allowing their persistence in a favorable environment (Dang and Lovell 2000; Flemming and Wingender 2001). EPSs are also being applied as bioremediation agents in environmental management systems (Kavita et al. 2011) and in ecological studies, for example, the settlement of zoospores of algae and invertebrate larvae (Hadfield 2011; Singh et al. 2013; Othmani et al. 2016). Bacterial EPS also has the capability to emulsify organic pollutants and provide healthy environments to support algal survival (Singh et al. 2013).
However, the parameters that define the macroalgal surface environment include metabolites from the alga itself, the existing resident microbial community and secondary metabolites of microbiological origin, as well as physical-chemical conditions at the thallus surface, such as oxygen and carbon dioxide, which can modify the surface pH (Egan et al. 2013). Many of these parameters are subjected to daily (Spilling et al. 2010; Dittami et al. 2016) and/or seasonal variations (Hellio et al. 2004; Bengtsson et al. 2010). In addition, macroalgal surfaces provide a habitat rich in organic material, such as reserve substances (alginate, laminarin, mannitol, and fucoidan) that are present in brown algae (Kita et al. 2016). The algae release great amounts of organic carbon at the surrounding environment, providing nutrients to the microorganisms and unleashing bacteria chemotactic behavior (Goecke et al. 2010).
While the macroalgae represent a niche with unique and selective properties, they also experiment with a range of benefic and harmful interactions with their symbiotic bacterial community (Egan et al. 2013). Considering the ecological importance, as well as macroalgal applications, there is a growing interest in these algae-bacteria interactions. However, few studies are devoted to investigating these associations with brown algae.
Mutualism relations between brown macroalgae and bacteria
Nutrition and growing factors
Epiphytic heterotrophic bacteria mineralize organic substrates, providing carbon dioxide, minerals, and, in some cases, fixed nitrogen and plant growth regulators to the macroalgae. The algae, in turn, produce organic substances and oxygen that are used by the epiphytic bacteria (Singh et al. 2011b; Singh and Reddy 2014).
Besides nutritional benefits, it has been demonstrated that the presence of certain bacteria is needed for the normal morphological development and growth of certain brown algae (Tapia et al. 2016) such as E. siliculosus (Le Bail et al. 2010). The endogenous capacity to produce such phytohormones that determined morphogenesis in these algae has a relation with the bacterial auxin (Provasoli and Carlucci 1974), similar work with other macroalgae (Prasad et al. 2010; Spoerner et al. 2012). Similarly, catalase production by the epiphytic Pseudoalteromonas porphyrae may regulate cell growth in Saccharina japonica (Dimitrieva et al. 2006).
Life cycle and morphologic development of macroalgae
Bacteria have a positive impact on the morphological development of several macroalgae species and their life cycle (Marshall et al. 2006; Egan et al. 2013; Twigg et al. 2013). Recently, Tapia et al. (2016) isolated nine strains of epiphyte bacteria of the brown alga Ectocarpus sp. culture and evaluated its effect on the morphology, reproduction, and secreted metabolites on axenic conditions and on co-culture with bacteria. Among isolated bacteria, six strains were capable of restoring the typical branched morphology and the reproduction characteristics of Ectocarpus sp. The bacteria belonged to phylum Proteobacteria and affected significantly the metabolites released by the brown algae. Goecke et al. (2012) observed the presence of bacteria on the surface of the oogonia released from the brown algae Fucus vesiculosus. Due to the smaller size of the oogonia, bacterial degradation of unviable spores cannot be excluded. Thus, bacterial biofilms can play a role in spore release, germination, and subsequent colonization of substrates by algae. It was also observed that the bacterial biofilm plays an important role on spore germination and consequently on the colonization of new substrates by macroalgae, reporting a positive correlation between the zoospore settlement and the increase in density of the biofilm (Singh et al. 2015; Vesty et al. 2015). This fact suggests the importance of the biofilm on the recruiting of macroalgal communities in coastal environments. The impact of microorganisms on the life cycle and colonization process may be important in regulating algal populations that should be investigated. However, the effect of bacteria over algal gametes and spores remains extremely neglected. Whether or not those bacteria play a role in algal ecology is completely unknown with regard to brown algae.
Macroalgae and fouling defense
Many sessile eukaryotes are intimately associated with bacteria that enable them to expand their physiological capabilities. Associations between algae and bacteria have been described for over 100 years, and these interactions can be positive, neutral, or negative (Ainsworth et al. 2010; Hollants et al. 2013). There are many laboratory studies which demonstrate that epiphyte bacteria have inhibitor activity against fouling organisms (Rao et al., 2007; Egan et al. 2008). Recently, anti-fouling and antimicrobial properties were observed on isolated bacterial strains from brown algae species (Al-Saif et al. 2014; Susilowati et al. 2015; Othmani et al. 2016).
It is worth noting that anti-fouling and antibacterial activities are found in a range of bacterial taxonomic groups. For example, the brown alga Saccharina latissima hosts more than 100 different bacteria strains that cover the phyla Proteobacteria, Bacteroidetes, Firmicutes, and Actinobacteria (Wiese et al. 2009). In addition, Murugan et al. (2012) studied 15 isolated bacteria from the Dictyota dichotoma and Chaetomorpha linoides algae biofilm, and found that eight belonged to the genera Pseudomonas, Bacillus, Corynebacterium, Micrococcus, Vibrio, Alteromonas, Flavobacterium, and Aeromonas. Furthermore, antibacterial and anti-fouling activities demonstrated by these algae can be attributed not only to the chemical defenses inherent in them but also with contribution through symbiosis or mutualistic association by epiphytic bacterial communities (Armstrong et al. 2001). This indicates that this association could both inhibit and induce the settlement of many organisms such as invertebrate larvae (Steinberg and de Nys 2002; Dworjanyn and Pirozzi 2008; Soares et al. 2008).
Bacteria-macroalgae harmful relationships
In consideration of the relationships between macroalgae and bacteria, there are advantages and disadvantages that have been investigated for over 20 years (Hollants et al. 2013). The microorganisms increasingly are known for their role as disease etiological agents in animals, plants, and marine algae (Egan et al. 2013). This interest in microbial disease in marine ecosystems is partially boosted by concerns related to climate change that generates stress on marine habitat formers and their associated microbiota which may make them more susceptible to potential opportunistic pathogens (Gachon et al. 2010).
Although there are some beneficial aspects of the associations between macroalgae and bacteria, the formation of biofilms can be a permanent threat to macroalgae. That is because biofilms may cause an increase in the host hydrodynamic resistance, reduce buoyancy and tissue elasticity, as well as attract herbivores and thus increase tissue loss or even result in its destruction (Vairappan et al. 2008, 2010). In addition, bacteria compete for nutrients (Goecke et al. 2010). The biofilm can also inhibit the gas exchange as well as reduce the availability of light, which can reduce algal photosynthetic activity. It may also increase the attachment and growth of a variety of other fouling organisms, like diatoms, invertebrate larvae, and other epiphyte algae spores. In addition, the host macroalga can be directly damaged by the bacterial community due to toxins, digestive enzymes, inhibitors, or waste products production, resulting in algal diseases (Huggett et al. 2006; Gachon et al. 2010).
In brown algae, the enrichment of some bacteria responsible for thallus rotting disease has been observed (Gachon et al. 2010). For example, Wang et al. (2008) cultivated a large number of bacteria from the thallus of S. japonica, which exhibited symptoms of the hole-rotten disease and found abundant Pseudoalteromonas and Vibrio bacteria. Studies of Laminaria religiosa health also revealed that Alteromonas bacteria are pathogenic and that they, allied with abiotic factors, induce severe damage and bleaching to the alga (Vairappan et al. 2001).
It is very likely that some of the bacteria found in the tissue of sick macroalgae are secondary colonizers that act as potential saprophytes or decomposers (Egan et al. 2013). Therefore, certain epiphytic bacteria might be commensal; however, but under stressful conditions or macroalgae infection, they become mainly saprophitic (Zozaya-Valdes et al. 2015).
Chemical interactions between bacteria and brown algae: potential new bioactives for new drugs
The marine environment represents a still unexploited resource for the isolation of novel bacterial and/or marine algal natural products such as antimicrobials (Uzair et al. 2018; Penesyan et al. 2010, 2011; Menaa 2015). The natural products chemistry of brown algae has been widely studied and they produce many types of volatile hydrocarbons, sterols, carotenoids, polyphenols, and unique terpenes (Cavalcanti et al. 2006; Moon et al. 2011; Mesquita et al. 2015). However, marine microorganisms are also seen as good candidates for the production of new compounds as potential drugs (Penesyan et al. 2010) and it is worth noting that practically all multicellular organisms that have been collected and extracted for chemical studies include associated microorganisms and this presents questions about the real biosynthetic origin of the isolated molecules (Goecke et al. 2010).
The bacterial communities associated with algae have specific characteristics when compared to bacterial strains isolated from other marine samples and are an extremely diverse potential source of bioactive compounds (Penesyan et al. 2010, 2011; Tujula et al. 2010; Burke et al. 2011; Penesyan et al. 2015). The bacterial communities associated with algae belong to several genera such as Pseudomonas, Pseudoalteromonas, Stenotrophomonas, Vibrio, Alteromonas, Shewanella, Streptomyces, and Bacillus, and have evolved in a highly competitive environment with nutrient and host space limitations, producing allelochemicals capable of preventing secondary colonization (Egan et al. 2008; Wiese et al. 2009). Marine bioactive compounds can provide wide protection (i.e., antibacterial, antifungal, antiviral, antiparasitic, antitumor, antioxidant) to the host (i.e., marine brown algae) against other microorganisms (Horta et al. 2014; Busetti et al. 2015; Uzair et al. 2018). As algae have no immune system and are continuously exposed to a range of biotic factors, they rely on secondary chemical defenses against fouling and potentially pathogenic microorganisms (see reviews by Steinberg and de Nys 2002; Goecke et al. 2010).
From 2010 until 2018, 35 studies have reported 61 species of brown algae showing bioactivities, with antibacterial activity the main activity (Fig. 3). The emphasis on antibacterial activity is because of the increase in multidrug-resistant bacteria driving the search for new substances to combat these pathogens (Meena et al. 2015). A larger number of studies have tested only crude extracts which contain a broad spectrum of natural products, hindering the identification of the particular chemical class or compound which is responsible for each activity. Few studies have isolated and identified such substances. For example, Uzair et al. (2018) isolated a new natural antibiotic (4-[(Z)-2 phenyl ethenyl] benzoic acid; Kocumarin), extracted from a new bacterium (Kocuria marina) which is associated with the brown alga Pelvetia canaliculata. In in vitro screens, Kocumarin inhibited all pathogenic fungi and bacteria tested and represents a potential new natural antibiotic for in vivo and environmental applications. Polyketides with antibacterial properties have been isolated from Bacillus subtilis associated with the brown algae Sargassum myriocystum and Anthophycus longifolius (Chakraborty et al. 2017, 2018). These studies have also suggested an ecological and metabolic role for these compounds in algal and bacteria associations. For example, Kubanek et al. (2003) have proposed that terpenoids such as lobophoride isolated from Lobophora variegata have a role in the alga’s defense against pathogenic and saprophytic fungi.
In addition to antibacterial activities, the ecological role of secondary metabolites on bacterial surface colonization also has been investigated demonstrating that the extracts and/or the isolated products acting on bacterial biofilm formation are very specific (Lachnit et al. 2010, 2013).
Marine macroalgae communicate via the surrounding environment and defend themselves by the production of metabolites. The communication between bacteria is through quorum sensing (QS), which is a chemically mediated language system that allows bacterial behavior coordination in relation to the environment (Joint et al. 2007). This system functions by the regulation of genes in response to population density. It also takes part in many physiological process such as cell differentiation, nutrient influx, bioluminescence, induction of virulence factors on pathogens of plants and animals, antibiotic biosynthesis, and biofilm formation (Bai and Rai 2011; Hollants et al. 2013).
Gram-negative bacteria, such as Pseudomonas and Vibrio, produce N-acyl homoserine lactones as signaling substances that pass through the cell membrane and bind to regulatory proteins inside the cell (Kalia 2013). Pseudomonas spp. are also known for the production of diketopiperazines that acts as QS signals (Dickschat 2010). Signaling molecules, such as γ-butyrolactones and oligopeptides, are synthetized by Gram-positive bacteria, such as Streptomyces and Bacillus (Dobretsov et al. 2009). Kanagasabhapathy et al. (2009) have suggested that certain epiphytic bacteria of the brown alga Colpomenia sinuosa play a role on the defense mechanism and suppress the settlement of other competitive bacteria, through the production of quorum sensing inhibitors (QSI) or substances similar to QSI. Macroalgae also can control bacterial colonization by interfering with the bacterial QS system as well as by the production of reactive oxygen species, similar to what happens in terrestrial plants (Potin 2008; Dittami et al. 2011). In the last decade, it has been shown that many macroalgae are capable of stimulating, inhibiting, or activating QS by bacteria through the production of QSI or analogous molecules (Kalia and Purohit 2011; Jha et al. 2013; Carvalho et al. 2017).
Another important point is that the QSI and antimicrobial substances produced by many epiphytic bacteria work together with the secondary metabolites from marine macroalgae to protect the host surface from pathogens, fouling organisms, and herbivores (Wiese et al. 2009). Many new compounds with antibiotic activities have been identified through brown algae-bacteria interaction (Horta et al. 2014; Martin et al. 2014). With the growing need to find new drugs, the understanding of marine epiphyte associations described should provide a rich source of new biomolecules of high value with the potential economic and sustainable human benefits (Murray et al. 2013; Martin et al. 2014). Therefore, bacteria associated with algae represent an important potential source of new substances (JanakiDevi et al. 2013) and are potentially easier to use in biotechnological applications when compared to a marine algal derivative (Manilal et al. 2010).
Conclusions and perspectives
Marine benthic environments are diverse and characterized by the constant competition of organisms for light, space, and nutrients. In these habitats, many macroalgae offer a substrate rich in organic material and also a safe habitat for bacterial (and other microorganisms) colonization and reproduction. The association between brown algae and bacteria can be mutualistic, a condition where the bacterial community protects the host against biological colonization, while the host surface can provide nutrients and physical protection to the bacteria. On the other hand, other types of associations can be disadvantageous to the algae, and could involve diseases, loss of the photosynthetic capability, and the costs associated with epiphytic growth.
Many studies have shown that biofilms play an important role in the development of macroalgal communities and that the bacterial communities communicate by QS. Therefore, the capability of exploring the bacterial sensorial system contributes to the understanding of the ecological success of algae. In addition, many macroalgae are capable of stimulating or inhibiting quorum sensing in bacteria. To tolerate the fouling organisms, algae have developed defense strategies that result in a great diversity of chemical substances, making them promising organisms as a source of bioactive biochemical actives, produced by either the algae or associated microorganisms. Although there is a growing interest in the secondary metabolites of the microorganisms associated with algae as a source of new natural and antimicrobial bioactive substances, little is known about the role these metabolites play in the mediation of such biological interactions.
In the last decades, the combined utilization of new microbiological, microscopy, and molecular biology techniques have helped significantly to identify and establish the phylogenetic affiliation of the algae-associated bacterial community. However, many questions about associated bacterial occurrence, distribution, persistence, and ecological roles remain unsolved, especially in studies concerning brown algae.
Many compounds with antibacterial activity have been identified from bacteria associated with brown algae. There is an urgency in finding new antibacterial substances from different natural sources, notably from the marine environment, which has organisms capable of synthesizing many unique chemical structures providing a new mechanism of action against new or reemerging infectious diseases. Therefore, future studies should observe not only the effect of specific pathogens but also the potential probiotic pathogenic effect of algae-bacteria interactions using the advances in new technologies.
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Acknowledgements
The first author is thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) for the PhD fellowship. This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). The authors also thank the collaboration of MSc. Ana Débora Nunes Pinheiro in the review of English and suggestions for this manuscript.
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de Mesquita, M.M.F., Crapez, M.A.C., Teixeira, V.L. et al. Potential interactions bacteria-brown algae. J Appl Phycol 31, 867–883 (2019). https://doi.org/10.1007/s10811-018-1573-4
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DOI: https://doi.org/10.1007/s10811-018-1573-4