Dataset Information

The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides.

ABSTRACT: In recent years, representatives of the Bacteroidetes have been increasingly recognized as specialists for the degradation of macromolecules. Formosa constitutes a Bacteroidetes genus within the class Flavobacteria, and the members of this genus have been found in marine habitats with high levels of organic matter, such as in association with algae, invertebrates, and fecal pellets. Here we report on the generation and analysis of the genome of the type strain of Formosa agariphila (KMM 3901(T)), an isolate from the green alga Acrosiphonia sonderi. F. agariphila is a facultative anaerobe with the capacity for mixed acid fermentation and denitrification. Its genome harbors 129 proteases and 88 glycoside hydrolases, indicating a pronounced specialization for the degradation of proteins, polysaccharides, and glycoproteins. Sixty-five of the glycoside hydrolases are organized in at least 13 distinct polysaccharide utilization loci, where they are clustered with TonB-dependent receptors, SusD-like proteins, sensors/transcription factors, transporters, and often sulfatases. These loci play a pivotal role in bacteroidetal polysaccharide biodegradation and in the case of F. agariphila revealed the capacity to degrade a wide range of algal polysaccharides from green, red, and brown algae and thus a strong specialization of toward an alga-associated lifestyle. This was corroborated by growth experiments, which confirmed usage particularly of those monosaccharides that constitute the building blocks of abundant algal polysaccharides, as well as distinct algal polysaccharides, such as laminarins, xylans, and ?-carrageenans.

SUBMITTER: Mann AJ

PROVIDER: S-EPMC3811500 | biostudies-literature | 2013 Nov

REPOSITORIES: biostudies-literature

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The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides.

Mann Alexander J AJ Hahnke Richard L RL Huang Sixing S Werner Johannes J Xing Peng P Barbeyron Tristan T Huettel Bruno B Stüber Kurt K Reinhardt Richard R Harder Jens J Glöckner Frank Oliver FO Amann Rudolf I RI Teeling Hanno H

Applied and environmental microbiology 20130830 21

In recent years, representatives of the Bacteroidetes have been increasingly recognized as specialists for the degradation of macromolecules. Formosa constitutes a Bacteroidetes genus within the class Flavobacteria, and the members of this genus have been found in marine habitats with high levels of organic matter, such as in association with algae, invertebrates, and fecal pellets. Here we report on the generation and analysis of the genome of the type strain of Formosa agariphila (KMM 3901(T)) ...[more]

PMID: 23995932

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Project description:Flavobacteriia are recognized as key players in the marine carbon cycle, due to their ability to efficiently degrade algal polysaccharides both in the open ocean and in coastal regions. The chemical complexity of algal polysaccharides, their differences between algal groups and variations through time and space, imply that marine flavobacteria have evolved dedicated degradation mechanisms and regulation of their metabolism during interactions with algae. In the present study, we report the first transcriptome-wide gene expression analysis for an alga-associated flavobacterium during polysaccharide degradation. Zobellia galactanivorans DsijT, originally isolated from a red alga, was grown in minimal medium with either glucose (used as a reference monosaccharide) or one selected algal polysaccharide from brown (alginate, laminarin) or red algae (agar, porphyran, ?- or ?-carrageenan) as sole carbon source. Expression profiles were determined using whole-genome microarrays. Integration of genomic knowledge with the automatic building of a co-expression network allowed the experimental validation of operon-like transcription units. Differential expression analysis revealed large transcriptomic shifts depending on the carbon source. Unexpectedly, transcriptomes shared common signatures when growing on chemically divergent polysaccharides from the same algal phylum. Together with the induction of numerous transcription factors, this hints at complex regulation events that fine-tune the cell behavior during interactions with algal biomass in the marine environment. The results further highlight genes and loci that may participate in polysaccharide utilization, notably encoding Carbohydrate Active enZymes (CAZymes) and glycan binding proteins together with a number of proteins of unknown function. This constitutes a set of candidate genes potentially representing new substrate specificities. By providing an unprecedented view of global transcriptomic responses during polysaccharide utilization in an alga-associated model flavobacterium, this study expands the current knowledge on the functional role of flavobacteria in the marine carbon cycle and on their interactions with algae.

Project description:Marine bacteria play important roles in the degradation and cycling of algal polysaccharides. However, the dynamics of epiphytic bacterial communities and their roles in algal polysaccharide degradation during kelp decay are still unclear. Here, we performed metagenomic analyses to investigate the identities and predicted metabolic abilities of epiphytic bacterial communities during the early and late decay stages of the kelp Saccharina japonica. During kelp decay, the dominant epiphytic bacterial communities shifted from Gammaproteobacteria to Verrucomicrobia and Bacteroidetes. In the early decay stage of S. japonica, epiphytic bacteria primarily targeted kelp-derived labile alginate for degradation, among which the gammaproteobacterial Vibrionaceae (particularly Vibrio) and Psychromonadaceae (particularly Psychromonas), abundant in alginate lyases belonging to the polysaccharide lyase (PL) families PL6, PL7, and PL17, were key alginate degraders. More complex fucoidan was preferred to be degraded in the late decay stage of S. japonica by epiphytic bacteria, predominantly from Verrucomicrobia (particularly Lentimonas), Pirellulaceae of Planctomycetes (particularly Rhodopirellula), Pontiellaceae of Kiritimatiellota, and Flavobacteriaceae of Bacteroidetes, which depended on using glycoside hydrolases (GHs) from the GH29, GH95, and GH141 families and sulfatases from the S1_15, S1_16, S1_17, and S1_25 families to depolymerize fucoidan. The pathways for algal polysaccharide degradation in dominant epiphytic bacterial groups were reconstructed based on analyses of metagenome-assembled genomes. This study sheds light on the roles of different epiphytic bacteria in the degradation of brown algal polysaccharides.IMPORTANCEKelps are important primary producers in coastal marine ecosystems. Polysaccharides, as major components of brown algal biomass, constitute a large fraction of organic carbon in the ocean. However, knowledge of the identities and pathways of epiphytic bacteria involved in the degradation process of brown algal polysaccharides during kelp decay is still elusive. Here, based on metagenomic analyses, the succession of epiphytic bacterial communities and their metabolic potential were investigated during the early and late decay stages of Saccharina japonica. Our study revealed a transition in algal polysaccharide-degrading bacteria during kelp decay, shifting from alginate-degrading Gammaproteobacteria to fucoidan-degrading Verrucomicrobia, Planctomycetes, Kiritimatiellota, and Bacteroidetes. A model for the dynamic degradation of algal cell wall polysaccharides, a complex organic carbon, by epiphytic microbiota during kelp decay was proposed. This study deepens our understanding of the role of epiphytic bacteria in marine algal carbon cycling as well as pathogen control in algal culture.

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Dataset Information

The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides.

Publications

The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides.

Similar Datasets

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