The Genome of the Alga-Associated Marine Flavobacterium Formosa agariphila KMM 3901 ^T 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.

Microbial Surface Colonization and Biofilm Development in Marine Environments

“…Studies have shown that Bacteroidetes bacteria are common in marine environments (791), abundant in organic particle-rich coastal waters (108,113,130,611,791), responsive to algal and jellyfish blooms (272,537,756,(791)(792)(793), copiotrophic (252), and prone to leading a surface-associated life (12,17,246,272,574,607) supported by the extracellular degradation of complex biopolymers such as polysaccharides and proteins (194,791,(794)(795)(796)(797). These bacteria harbor a large number of genes for adhesive exopolysaccharides, adhesion proteins, proteases, peptidases, glycoside hydrolases, and lipases, and several genes for biopolymer degradation are coregulated with the genes for TonBdependent transport systems (794,795,(798)(799)(800)(801)(802). These properties indicate that the marine Bacteroidetes are specialists in surface colonization and play a key role in the degradation and utilization of HMW DOM and POM (272,791).…”

Proteomics analysis of the response of the marine bacterium Marinobacter adhaerens HP15 to the diatom Thalassiosira weissflogii

“…In support of this, the proteomics approach did not show any carbohydrate uptake systems or carbohydrate-utilizing proteins being upregulated in M. adhaerens HP15 in the presence of the diatom. The findings were further substantiated by the remarkably low number of carbohydrate utilization-associated proteins encoded by the genome of M. adhaerens HP15, as compared to those of classical degraders of algae exudates, such as Flavobacterium johnsoniae UW101 (McBride et al 2009) or other members of the Flavobacteria (Mann et al 2013).…”

“…Consequently, the majority of these carbohydrates were considered experimentally in the present study. Certain bacterial groups, such as members of the Bacteroidetes, are known for their ability to degrade carbohydrate compounds resulting from algae exudates (Teeling et al 2012, Mann et al 2013). According to our proteomics and carbon utilization results, none of the tested carbohydrates was used as a carbon source by M. adhaerens HP15 except for fructose.…”

Perspectives on the microbial carbon pump with special reference to microbial respiration and ecosystem efficiency in large estuarine systems

“…Bacteroidetes are particularly rich in carbohydrate-assimilation TBDT (Blanvillain et al, 2007;González et al, 2008;Hehemann et al, 2010;Tang et al, 2012) and biopolymer degradation enzymes (McBride et al, 2009;Hehemann et al, 2010;Qin et al, 2010;Thomas et al, 2012;Mann et al, 2013). Many Bacteroidetes glycoside hydrolase genes are organized in polysaccharide utilization loci, usually clustered with genes for TonB-dependent receptors, SusD-like proteins, sensors/transcription factors, transporters and frequently with genes for sulfatases (McBride et al, 2009;Hehemann et al, 2010;Qin et al, 2010;Thomas et al, 2012;Fernández-Gómez et al, 2013;Mann et al, 2013).…”

“…Environmental sequences of Bacteroidetes TBDT-related proteins, genes and their transcripts have been frequently found in abundance in metaproteomic, metagenomic and metatranscriptomic sequences from various ocean habitats, especially in coastal waters (Morris et al, 2010;Ottesen et al, 2011;Tang et al, 2012). Bacteroidetes also harbor diverse genes for the degradation of proteins, chitin and bacterial cell wall peptidoglycans (Cottrell and Kirchman, 2000;McBride et al, 2009;Qin et al, 2010;Gómez-Pereira et al, 2012;Mann et al, 2013). Thus, Bacteroidetes have been regarded as specialists for degradation of HMW biomacromolecules in both the particulate and dissolved fraction of the marine OM pool (Bauer et al, 2006).…”