A Functional Perspective Analysis of Macroalgae and Epiphytic Bacterial Community Interaction

Abstract

Macroalgae are photosynthetic, multicellular, sessile eukaryotic organisms that offer diverse habitats for the colonization of epiphytic bacteria, therefore establishing biological interactions of diverse complexity. This review focusses on the interactions between macroalgae and their Epiphytic Bacterial Community (EBC); the main aims are to ascertain whether (1) the epiphytic bacterial groups differ at the phylum and genus levels of the macroalgae; (2) the methodologies used so far to study these microorganisms are related in any way to eventual variations of the EBCs on macroalgae; and (3) the EBC of macroalgae has a functional means rather a simple taxonomic grouping. Results showed firstly the taxonomic grouping of macroalgae does not explain the composition and structure of the EBCs. Secondly, the methodology used is important for describing EBCs; and thirdly, multiple bacteria can have the same function and thus to describe the functionality of EBCs it is important to recognize host-specific and generalist bacteria. We recommend the incorporation of a complementary approach between the taxonomic composition and the functional composition analyzes of EBCs, as well as the use of methodological tools that allow analysis of interactions between the EBCs and their hosts, based on the "holobiont" concept.

Keywords: biological interactions; epiphytic bacteria; holobiont; host-specific; macroalgae.

Figure 1

Comparison of phyla of epiphytic bacteria reported for the different phyla of macroalgae (Chlorophyta, Heterokontophyta, and Rhodophyta). Proteobacteria classes were included because some articles included this taxonomic level. The percentage values were calculated based on the total number of bacterial phyla found in the literature consulted (n = 25) and represented in a Venn Diagram to indicate the bacteria that are shared among macroalgal phyla, as well as the methodology used in each of the 25 studies (Table S1).

Figure 2

Abundance and distribution of epiphytic bacteria, at the level of phylum and class of Proteobacteria, associated to macroalgal genera of the different macroalgal phyla: Chlorophyta (C), Heterokontophyta (H), and Rhodophyta (R). Proteobacteria classes were included because some articles included this taxonomic level. The scale in the upper left shows the correspondence between colors and abundance values of bacteria. Abundance was defined as the number of Presences/Absences of epiphytic bacteria reported for each macroalgal genus in the literature consulted (n = 32). The bacterial phyla were ordered from highest to lowest abundance value. “Unclassified” are microorganisms that could not be classified in any group. “Unidentified” classified as bacteria, but could not be strongly identified. Taxonomic classification corresponded to those used in the literature consulted (Tables S2, S3).

Figure 3

Relative abundance of rare epiphytic bacteria, at the phylum level and class of Proteobacteria, associated to macroalgal genera of the different macroalgal phyla: Chlorophyta (C), Heterokontophyta (H), and Rhodophyta (R). Proteobacteria classes were included because some articles included this taxonomic level. Rare epiphytic bacteria were defined as those that were only mentioned once in the literature consulted. The percentage values for each bacterial phylum were calculated in relation to the total number of rare epiphytic bacteria associated with each macroalgal genus according to the literature consulted (n = 32). Bacterial phyla were ordered from more to less common among macroalgal genus. The taxonomic classification corresponded to those used in the literature consulted (Table S4).

Figure 4

Abundance and distribution of epiphytic bacteria, at the family level, associated to macroalgal genera of the different macroalgal phyla: Chlorophyta (C), Heterokontophyta (H), and Rhodophyta (R). The scale in the upper left shows the correspondence between colors and abundance values of bacteria. Abundance was defined as the number of Presence/Absences of epiphytic bacteria, at the family level, reported for each macroalgal genus in the literature consulted (n = 32). The bacterial family were ordered from highest to lowest abundance value. Taxonomic classification corresponded to those used in the literature consulted (Table S5).

Figure 5

Abundance and distribution of epiphytic bacteria, at the family level, associated to the different methodological approaches: Culture-Dependent Methods (CDM), Molecular Methods (MM), Culture-Dependent Methods and Molecular Methods (CDM + MM), Pyrosequencing and Illumina (Mi-Seq). The scale in the upper left shows the correspondence between colors and abundance values of bacteria. Abundance was defined as the number of Presence/Absences of epiphytic bacteria, at the family level, reported for each methodological approach in the literature consulted (n = 32). The bacterial family were ordered from highest to lowest abundance value. Taxonomic classification corresponded to those used in the literature consulted (Table S6).

Figure 6

Reports in the literature of the effects associated with epiphytic bacteria in macroalgal phyla: Chlorophyta (C), Heterokontophyta (H), and Rhodophyta (R). The effects correspond to: Inducing morphogenesis (IM), Pathogen (P), Spore release (SR), Stimulation settlement of algal spores (SS), Prevent settlement of algal spores (PS), Antifouling (A), Antibacterial activity and Degradation of algal compounds (DC). The percentage values for each macroalgal phylum were calculated in relation to the total number of papers reviewed (n = 25), and the percentages of each effect for each macroalgal phylum were added. The macroalgal phyla were arranged in alphabetical order (Table S7).

Figure 7

Effects associated with epiphytic bacterial families in macroalgae. The effects correspond to: Inducing morphogenesis (IM), Pathogen (P), Spore release (SR), Stimulation settlement of algal spores (SS), Prevent settlement of algal spores (PS), Antifouling (A), Antibacterial activity (AB) and Degradation of algal compounds (DC). Percentage values for each bacterial family were calculated relative to the number of papers reviewed for each function (n-values presented in the graph). The bacterial family were ordered from lowest to highest percentage value. Taxonomic classification corresponded to those used in the literature consulted (Tables S8, S9).