Overview of the taxonomy and of the major secondary metabolites and their biological activities related to human health of the Laurencia complex (Ceramiales, Rhodophyta) from Brazil

Overview of the taxonomy and of the major secondary metabolites and their biological activities related to human health of the Laurencia complex (Ceramiales, Rhodophyta) from Brazil

Mutue T. Fujii^I,*; Valéria Cassano^II; Érika M. Stein^III; Luciana R. Carvalho^I

^INúcleo de Pesquisa em Ficologia, Instituto de Botânica, Brazil

^IIDepartamento de Botânica, Universidade de São Paulo, Brazil

^IIIPrograma de Pós-graduação, Departamento de Botânica, Universidade de São Paulo, Brazil

ABSTRACT

In Brazil, the Laurencia complex is represented by twenty taxa: Laurencia s.s. with twelve species, Palisada with four species (including Chondrophycus furcatus now that the proposal of its transference to Palisada is in process), and Osmundea and Yuzurua with two species each. The majority of the Brazilian species of the Laurencia complex have been phylogenetically analyzed by 54 rbcL sequences, including five other Rhodomelacean species as outgroups. The analysis showed that the Laurencia complex is monophyletic with high posterior probability value. The complex was separated into five clades, corresponding to the genera: Chondrophycus, Laurencia, Osmundea, Palisada, and Yuzurua. A bibliographical survey of the terpenoids produced by Brazilian species showed that only six species of Laurencia and five of Palisada (including C. furcatcus) have been submitted to chemical analysis with 48 terpenoids (47 sesquiterpenes and one triterpene) isolated. No diterpenes were found. Of the total, 23 sesquiterpenes belong to the bisabolane class and eighteen to the chamigrene type, whose biochemical precursor is bisabolane, two are derived from lauranes and four are triquinols. Despite the considerable number of known terpenes and their ecological and pharmacological importance, few experimental biological studies have been performed. In this review, only bioactivities related to human health were considered.

Keywords: biodiversity, biological activities, Laurencia complex, seaweeds, taxonomy, terpenoids

Introduction

The red algae of the Laurencia complex comprehend 430 species (and infraspecific taxa) listed in the database at present, of which 134 have been flagged as currently accepted taxonomically. They are reported worldwide from the temperate to tropical shores of the world, occurring from the intertidal to the subtidal zone up to 65 m in depth (Guiry & Guiry, 2010). Laurencia sensu lato is an extremely rich source of halogenated secondary metabolites with diverse structural features (Fenical, 1975; Erickson, 1983) that can be divided into two groups according to their biogenetic origin. The first one is the nonterpenoid group, which contains the acetogenins derived from the metabolism of fatty acids. The other one is the terpenoid group, in which the sesquiterpenes are the most abundant, but also containing diterpenes and triterpenes (Fernández et al., 2005).

The taxonomy of the Laurencia complex has undergone several changes based on the use of new vegetative morpho-anatomical and reproductive features, cladistic analyses of morphological characters and molecular approaches based on the plastidial rbcL gene (Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006, 2007; Martin-Lescanne et al., 2010). These changes include the resurrection of the genus Osmundea Stackhouse (Nam et al., 1994), the elevation of the subgenus Chondrophycus Tokida & Saito (in Saito, 1967) to the generic rank (Garbary & Harper, 1998), the new delineations of the genera Chondrophycus, Laurencia and Osmundea (Nam, 1999), the definition of the proposal of the genus Palisada (Yamada) K.W. Nam based on Yamada's (1931) section Palisadae (Nam, 2006) and its later validation (Nam, 2007), and the establishment of the genus Yuzurua (K.W. Nam) Martin-Lescanne based on Nam's (1999) subgenus Yuzurua (Martin-Lescanne et al., 2010). Thus, five genera are currently assigned to the Laurencia complex: Laurencia J.V. Lamouroux itself, Osmundea, Chondrophycus, Palisada and Yuzurua. Several morpho-anatomical and reproductive characters used in the taxonomy of the complex have been shown to have diagnostic value at the generic level only (Saito, 1967; Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006). Many species have no defined taxonomic boundaries and present extensive morphological plasticity, making their taxonomic delimitation difficult. In this context, the use of molecular markers has proven to be useful for delimiting the taxa and inferring their phylogenetic relationships and has corroborated the current classification system (Nam et al., 2000; McIvor et al., 2002; Abe et al., 2006; Fujii et al., 2006; Díaz-Larrea et al., 2007; Cassano et al., 2009; Gil-Rodríguez et al., 2009; Martin-Lescanne et al., 2010; Rocha-Jorge et al., 2010).

The genera are distinguished by a combination of both vegetative and reproductive characteristics: number of pericentral cells per vegetative axis, position of the first pericentral cell relative to the trichoblast, origin of the tetrasporangia, absence or presence of fertility of the second pericentral cell, number of sterile pericentral cells in the tetrasporangial axis, origin of the spermatangial branches, formation pattern of the spermatangial branches on trichoblasts, the number of pericentral cells in procarp-bearing segments of female trichoblasts, and probably post-fertilization features associated with the formation time of the auxiliary cell. Many of these characters overlap among the genera. Effectively, the genus Laurencia is distinct from the other four genera by the presence of four pericentral cells per axial segment; two pericentral cells occur in Osmundea, Chondrophycus, Palisada and Yuzurua (Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006; Martin-Lescanne et al., 2010). The genus Osmundea is distinct from the other genera by the tetrasporangial production from random cortical cells rather than from particular pericentral cells and filament-type rather than trichoblast-type spermatangial development (Nam et al., 1994). The genus Chondrophycus is characterized by spermatangial branches produced from two laterals on the suprabasal cell of trichoblasts, but remaining partly sterile, and a tetrasporangial axis with the first and second pericentral cells never fertile (Nam, 1999). In the genus Palisada, the spermatangial branches are produced from one of two laterals on the suprabasal cells of trichoblasts and the second pericentral cell in the tetrasporangial axis is always fertile; the resulting axis has one sterile pericentral cell (Nam, 2006). The genus Yuzurua shares the majority of the morphological characters of Palisada, from which it was recently segregated, but differs by not having palisade-like cells, by the presence of secondary pit-connections between cortical cells, and by procarp-bearing segments with five pericentral cells rather than four (Fujii et al., 1996).

The species of the Laurencia complex are widely distributed along the Brazilian coast from Ceará (Pinheiro-Joventino et al., 1998) to Rio Grande do Sul (Baptista, 1977), growing in different types of habitats (Fujii & Sentíes, 2005) and constituting an important element of Brazilian phycological flora (Oliveira Filho, 1977).

The members of this complex, in particular Laurencia s.s., are prolific synthesizers of structurally elaborate halogenated secondary metabolites and have been reported to produce a numerous diversity of unique compounds, especially terpenes (Martín & Darias, 1978; Erickson, 1983; Pereira & Teixeira, 1999). Although the function of these secondary metabolites has not yet been clearly defined, it has been suggested that these metabolites play a major role in mediating ecological interactions such as algae/herbivore interactions (Hay et al., 1987, Hay & Steinberg, 1992), with these compounds acting as a defense against being eaten or as a deterrent against epibiota, i.e., an antifouling activity (da Gama et al., 2002; Cassano et al., 2008; Lhullier et al., 2009), or protection against pathogens (König & Wright, 1997). Thus, ecological pressures such as competition for space, fouling of the surface, predation, and successful reproduction have led to the evolution of unique secondary metabolites with various biological activities (Ireland et al., 2000). The prominent biological activity of marine terpenes is evident in their ecological role in the marine environment and makes them interesting as potential drugs. Many of these natural products are pharmacologically active and marine algae, especially those from tropical and subtropical seas, are able to produce a wide range of compounds, many of which exhibit at least some degree of bioactivity (Fernández et al., 1998, 2005; da Gama et al., 2002; Cassano et al., 2008; Lhullier et al., 2009; Machado et al., 2010; Santos et al., 2010). In fact, the marine environment represents a treasure trove of useful products awaiting discovery for the treatment of infectious and parasitic diseases (Vairappan et al., 2004; Morales et al., 2006), cancer (Mohammed et al., 2004; Stein et al., 2011), cognitive diseases, inflammatory processes, and viral infections (Sakemi et al., 1986). Despite the many structures known and their ecological and pharmacological importance, only a few biosynthetic studies have been performed on marine terpenoid compounds (Gross & König, 2006). In this paper, the current status of the taxonomy of the Laurencia complex in Brazil is outlined, together with the diversity of secondary metabolites produced and their biological activities of relevance to human health.

Materials and Methods

The present work is a compilation of the data on the Laurencia complex from Brazil, including the current results on the taxonomy and phylogeny of the group, secondary metabolites and their biological activities related to human health.

We performed a phylogenetic analysis using 54 rbcL sequences, with seventeen samples from Brazil (Table 1). Multiple alignments for sequences were constructed using the computer program BioEdit 7.0.4.1 (Hall, 1999). A total of 250 nucleotides were removed from all rbcL sequences at the beginning and end of the sequences because many sequences from the GenBank were incomplete, producing a data set of 1217 base pairs. Phylogenetic relationships were inferred with MrBayes v.3.0 beta 4 (Huelsenbeck & Ronquist, 2001). The model used in the Bayesian analysis was selected based on maximum likelihood ratio tests implemented by the software Modeltest version 3.06 (Posada & Crandall, 1998) with a significance level of 0.01 by the Akaike information criterion. For the Bayesian analysis, four chains of the Markov chain Monte Carlo (one hot and three cold) were used, sampling one tree every ten generations for 1,000,000 generations starting with a random tree. The 50,000 generations were discarded as 'burn in'. The model used in the Bayesian analysis for rbcL sequences was the general-time-reversible model of nucleotide substitution with invariant sites and gamma distributed rates for the variable sites (GTR+I+G).

Results and Discussion

In Brazil, the red algae of the Laurencia complex are represented by four of the five genera that integrate the complex: Laurencia itself, Palisada, Osmundea, and Yuzurua. The first is the most diverse with twelve species, followed by Palisada (including Chondrophycus furcatus) with four species and Osmundea and Yuzurua with two species each (Table 2). The habit of several representatives of the Laurencia complex from Brazil and some generic morphological diagnostic characters are displayed in Figures 1-²⁵.

The topology of the Bayesian tree with corresponding Bayesian posterior probabilities values (PP) is shown in Figure 26. The phylogenetic analysis shows a monophyletic Laurencia complex with high PP support (100%) in relation to the members of the outgroup, corroborating the previous results verified for the group (Abe et al., 2006; Fujii et al., 2006; Martin-Lescanne et al., 2010). The Laurencia complex was separated into five clades, corresponding to the genera: Laurencia, Osmundea, Palisada, Chondrophycus, and Yuzurua. The earliest diverging clade was the genus Palisada with six species and high support (100% PP), which included also Chondrophycus furcatus, an endemic species from Brazil. This result shows clearly that C. furcatus must be transferred to the genus Palisada and, with its future nomenclatural change, there will be no more representatives of Chondrophycus in Brazil. The monophyletic genera Chondrophycus and Osmundea were sister groups with a posterior probability of 86%. The monophyletic clade that corresponds to the genus Yuzurua showed higher molecular affinity with Laurencia than Palisada, from which it was recently segregated. The genus Laurencia included fifteen taxa with a posterior probability of 80%. Laurencia marilzae formed a monophyletic clade with high support (100% PP) and was separated from all other Laurencia s.s., forming a distinct lineage, suggesting that L. marilzae represents a new genus within the Laurencia complex.

The bibliographical survey on the terpenoids produced by species of the Laurencia complex from the Brazilian coast shows that only five species of Laurencia and three of Palisada (including C. furtactus) have been submitted to chemical analysis and that, so far, 48 terpenoids have been isolated: 47 sesquiterpenes and one triterpene. Diterpenes have not been found in Brazilian species (Table 3).

The compounds isolated from the native algae include 21 sesquiterpenes belonging to the bisabolane class, seventeen belonging to the chamigrane type, whose biochemical precursor is bisabolane, and four triquinols, that posses a rare structure but are derived from the same biogenetic origin as the bisabolane- and chamigrane-derived terpenoids [2E,6E-farnesylpyrophosphate (FPP)]. Besides bisabolane and chamigrane terpenoids, the introduced seaweed Laurencia caduciramulosa produces two laurane-type compounds not found in Brazilian native algae (Table 3).

With respect to Palisada perforata and P. flagellifera, they generally do not produce sesquiterpenoids or acetogenins, classical metabolites produced by Laurencia. Although the presence of sesquiterpenes was not expected in this group, triquinane alcohols (compounds 47 and 26) were found in P. perforata by using a high sensitivity extraction method (HS-SPME) (Gressler et al., 2011). These compounds were not active against bacterial strains or the yeast Candida albicans, but showed some antioxidant activity. Chondrophycus furcatus is distinct from the other members of Palisada by producing only triterpenoids (Rodriguez-Concepción, 2006) that are synthesized via the same precursor (FPP) as the sesquiterpenoids from Brazilian Laurencia species. However, on the basis of morphology, it does not fit perfectly into either Laurencia or Palisada due to the presence of secondary pit-connections between adjacent cortical cells, a characteristic more related to Laurencia, and to the production of two pericentral cells, instead of four per each axial segment, a characteristic shared by Chondrophycus, Palisada, Yuzurua and Osmundea (Fujii & Sentíes, 2005).

Most of the metabolites (15) that have been isolated from Laurencia dendroidea, L. scoparia, L. microcladia, and L. obtusa [denominations that, in Brazil, refer to the same botanical species (Cassano, 2009)] are derived from chamigrane, with very similar or even identical structures, such as elatol found in L. dendroidea and L. microcladia; L. scoparia produces five sesquiterpenoids from bisabolane and two triquinols. Both L. aldingensis and L. catarinensis synthesize metabolites whose precursor is bisabolane, exhibiting a high degree of similarity between them, as can be seen in Figure 26.

Although species of the Laurencia complex are known to produce interesting active metabolites that possess important pharmacological potential, experimental biological activity assays have been performed with only with six species: Laurencia catarinensis, L. dendroidea, L. translucida, L. aldingensis, L. caduciramulosa, and Palisada flagellifera. The three former are native Brazilian species and the most studied of these is L. dendroidea. More than twenty compounds were identified in this species and several of them showed biological activities such as anthelmintic activity against the parasitic stage of Nippostrongilus brasiliensis (Davyt, 2003; 2006), antileishmanial activity against the insect-stage promastigotes of Leishmania amazonensis (Machado et al., 2010), human pathogenic antifungal properties (Stein et al., 2011), and significant levels of toxicity towards a model tumor cell line (human uterine sarcoma, MES-SA) (Stein et al., 2011). Thus, studies on the biological activities of the secondary metabolites isolated from the Laurencia complex should be encouraged with the goal of finding new sources with pharmaceutical applications.

Acknowledgements

This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Proc. 473322/2008-0), and the Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. 10/50193-1, Proc. 10/52244-2). Additional support was provided by the Ministerio de Ciencia e Innovación of the Spanish Government (CGL 2010-14881). MT Fujii thanks the CNPq for a Research Productivity Fellowship (Proc. 301438/2009-9) and EM Stein thanks FAPESP for a Master's Student Fellowship (Proc. 2008/07775-0). Beneficiary of financial support from CAPES-Brazil.

Received 23 Dec 2010

Accepted 22 Jan 2011

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Publication Dates

• Publication in this collection
  20 Apr 2011
• Date of issue
  Apr 2011

History

• Received
  23 Dec 2010
• Accepted
  22 Jan 2011