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The Cultivable Surface Microbiota of the Brown Alga Ascophyllum nodosum is Enriched in Macroalgal-Polysaccharide-Degrading Bacteria - PubMed Skip to main page content
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. 2015 Dec 24:6:1487.
doi: 10.3389/fmicb.2015.01487. eCollection 2015.

The Cultivable Surface Microbiota of the Brown Alga Ascophyllum nodosum is Enriched in Macroalgal-Polysaccharide-Degrading Bacteria

Marjolaine Martin  1 , Tristan Barbeyron  2 , Renee Martin  1 , Daniel Portetelle  1 , Gurvan Michel  2 , Micheline Vandenbol  1
Affiliations

The Cultivable Surface Microbiota of the Brown Alga Ascophyllum nodosum is Enriched in Macroalgal-Polysaccharide-Degrading Bacteria

Marjolaine Martin et al. Front Microbiol. .

Abstract

Bacteria degrading algal polysaccharides are key players in the global carbon cycle and in algal biomass recycling. Yet the water column, which has been studied largely by metagenomic approaches, is poor in such bacteria and their algal-polysaccharide-degrading enzymes. Even more surprisingly, the few published studies on seaweed-associated microbiomes have revealed low abundances of such bacteria and their specific enzymes. However, as macroalgal cell-wall polysaccharides do not accumulate in nature, these bacteria and their unique polysaccharidases must not be that uncommon. We, therefore, looked at the polysaccharide-degrading activity of the cultivable bacterial subpopulation associated with Ascophyllum nodosum. From A. nodosum triplicates, 324 bacteria were isolated and taxonomically identified. Out of these isolates, 78 (~25%) were found to act on at least one tested algal polysaccharide (agar, ι- or κ-carrageenan, or alginate). The isolates "active" on algal-polysaccharides belong to 11 genera: Cellulophaga, Maribacter, Algibacter, and Zobellia in the class Flavobacteriia (41) and Pseudoalteromonas, Vibrio, Cobetia, Shewanella, Colwellia, Marinomonas, and Paraglaceciola in the class Gammaproteobacteria (37). A major part represents likely novel species. Different proportions of bacterial phyla and classes were observed between the isolated cultivable subpopulation and the total microbial community previously identified on other brown algae. Here, Bacteroidetes and Gammaproteobacteria were found to be the most abundant and some phyla (as Planctomycetes and Cyanobacteria) frequently encountered on brown algae weren't identified. At a lower taxonomic level, twelve genera, well-known to be associated with algae (with the exception for Colwellia), were consistently found on all three A. nosodum samples. Even more interesting, 9 of the 11 above mentioned genera containing polysaccharolytic isolates were predominant in this common core. The cultivable fraction of the bacterial community associated with A. nodosum is, thus, significantly enriched in macroalgal-polysaccharide-degrading bacteria and these bacteria seem important for the seaweed holobiont even though they are under-represented in alga-associated microbiome studies.

Keywords: Ascophyllum nodosum; Flavobacteriia; Gammaproteobacteria; agarase; algal polysaccharidase; alginate lyase; carrageenase; macroalgae.

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Figures

Figure 1
Figure 1
PCoA of the genera found on the three alga samples. Bacterial classes are indicated in different colors. The size of each spot is proportional to the relative abundance of the genus indicated above or next to it. The closer a spot is to a sample name, the more abundant this genus is in that sample. The Genera common to just to samples are aligned along the gray arrows. The genera identified on the three samples (i.e., the common core) are in the gray shadowed circle.
Figure 2
Figure 2
Phylogenetic tree with the Flavobacteriaceae. 16S rRNA sequences of 120 representatives of the family Flavobacteriaceae were aligned with those of our 41 MAPD flavobacterial isolates. Sequences were manually curated and phylogenetic trees were constructed with these alignments using the Neighbor Joining Method. Evolutionary distances were calculated according to Kimura's two-parameter model using the gamma distribution (Kimura, 1980).
Figure 3
Figure 3
Phylogenetic tree with the Gammaproteobacteria. 16S rRNA sequence of 355 representatives of the class Gammaproteobacteria were aligned with those of our 37 MAPD Gammaproteobacterial isolates. Sequence were manually curated and phylogenetic trees were constructed with these alignments using the Neighbor Joining Method. Evolutionary distances were calculated according to Kimura's two-parameter model using the gamma distribution (Kimura, 1980).
Figure 4
Figure 4
(A) Percentage proportions of the most represented genera in the total isolated bacterial population (formula image) and of the MAPD isolates belonging to these genera in the whole set of 78 MAPD isolates (formula image); (B) Percentage proportions of MAPD isolates belonging to each MAPD-isolate-containing genus in the whole set of 78 MAPD isolates (formula image), with their activities on red (formula image) or brown seaweed galactans (formula image).
Figure 5
Figure 5
Ranges of 16S rRNA identity percentages for the identified MAPD isolates vs. known species. Two third of the MAPD isolates (< 98.65% 16S rRNA identities) likely represent novel species. Indeed, 97% is the commonly accepted threshold percentage at which two species can be distinguished and 98.65% is the threshold proposed by Kim et al. (2014) which have compared the average nucleotide identities of almost 7000 prokaryotic genomes and their 16S rRNA gene identities.
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