TY - JOUR
T1 - Comparative Genomic Analysis Indicates that Niche Adaptation of Terrestrial Flavobacteria Is Strongly Linked to Plant Glycan Metabolism
AU - Kolton, Max
AU - Sela, Noa
AU - Elad, Yigal
AU - Cytryn, Eddie
N1 - Funding Information:
Our results strongly support this notion, and we postulate that GHs may be accurate genomic predictors for identification of plant-associated flavobacteria . For example, SEED-defined functional cluster analyses (), as well as detailed analysis of the flavobacterial GH distributions (, , ), specifically designated the stream isolate F . rivuli [] as a member of the terrestrial clade, contrary to its apparent aquatic origin. This was supported by the presence of glycoside hydrolases GH78 and GH106 (, ), which are responsible for rhamnogalacturonan cleavage which is incorporated mainly into cell walls of all land plants [,]. The notion that F . rivuli is in essence soil-derived is supported by a previous microbial fingerprinting-based study that analyzed stream and soil flavobacterial communities from in and around the stream from which F . rivuli was isolated []. Based on these analyses the authors inferred that the flavobacterial stream community, originated from soil washout []. Conversely, functional and GH clustering (, ) placed F . antarcticum , originally isolated from an Antarctic soil [], within the aquatic clade, which is supported by the absence of GH78 and GH106 in this bacterium (, ). We hypothesize that this stems from the absence of terrestrial plants in the isolated environment, emphasizing the notion that terrestrial plant glycans dictate the arsenal of GH’s in the terrestrial flavobacterial clade.
PY - 2013/9/26
Y1 - 2013/9/26
N2 - Flavobacteria are important members of aquatic and terrestrial bacterial communities, displaying extreme variations in lifestyle, geographical distribution and genome size. They are ubiquitous in soil, but are often strongly enriched in the rhizosphere and phyllosphere of plants. In this study, we compared the genome of a root-associated Flavobacterium that we recently isolated, physiologically characterized and sequenced, to 14 additional Flavobacterium genomes, in order to pinpoint characteristics associated with its high abundance in the rhizosphere. Interestingly, flavobacterial genomes vary in size by approximately two-fold, with terrestrial isolates having predominantly larger genomes than those from aquatic environments. Comparative functional gene analysis revealed that terrestrial and aquatic Flavobacteria generally segregated into two distinct clades. Members of the aquatic clade had a higher ratio of peptide and protein utilization genes, whereas members of the terrestrial clade were characterized by a significantly higher abundance and diversity of genes involved in metabolism of carbohydrates such as xylose, arabinose and pectin. Interestingly, genes encoding glycoside hydrolase (GH) families GH78 and GH106, responsible for rhamnogalacturonan utilization (exclusively associated with terrestrial plant hemicelluloses), were only present in terrestrial clade genomes, suggesting adaptation of the terrestrial strains to plant-related carbohydrate metabolism. The Peptidase/GH ratio of aquatic clade Flavobacteria was significantly higher than that of terrestrial strains (1.7±0.7 and 9.7±4.7, respectively), supporting the concept that this relation can be used to infer Flavobacterium lifestyles. Collectively, our research suggests that terrestrial Flavobacteria are highly adapted to plant carbohydrate metabolism, which appears to be a key to their profusion in plant environments.
AB - Flavobacteria are important members of aquatic and terrestrial bacterial communities, displaying extreme variations in lifestyle, geographical distribution and genome size. They are ubiquitous in soil, but are often strongly enriched in the rhizosphere and phyllosphere of plants. In this study, we compared the genome of a root-associated Flavobacterium that we recently isolated, physiologically characterized and sequenced, to 14 additional Flavobacterium genomes, in order to pinpoint characteristics associated with its high abundance in the rhizosphere. Interestingly, flavobacterial genomes vary in size by approximately two-fold, with terrestrial isolates having predominantly larger genomes than those from aquatic environments. Comparative functional gene analysis revealed that terrestrial and aquatic Flavobacteria generally segregated into two distinct clades. Members of the aquatic clade had a higher ratio of peptide and protein utilization genes, whereas members of the terrestrial clade were characterized by a significantly higher abundance and diversity of genes involved in metabolism of carbohydrates such as xylose, arabinose and pectin. Interestingly, genes encoding glycoside hydrolase (GH) families GH78 and GH106, responsible for rhamnogalacturonan utilization (exclusively associated with terrestrial plant hemicelluloses), were only present in terrestrial clade genomes, suggesting adaptation of the terrestrial strains to plant-related carbohydrate metabolism. The Peptidase/GH ratio of aquatic clade Flavobacteria was significantly higher than that of terrestrial strains (1.7±0.7 and 9.7±4.7, respectively), supporting the concept that this relation can be used to infer Flavobacterium lifestyles. Collectively, our research suggests that terrestrial Flavobacteria are highly adapted to plant carbohydrate metabolism, which appears to be a key to their profusion in plant environments.
UR - http://www.scopus.com/inward/record.url?scp=84884613513&partnerID=8YFLogxK
U2 - 10.1371/journal.pone.0076704
DO - 10.1371/journal.pone.0076704
M3 - Article
C2 - 24086761
AN - SCOPUS:84884613513
SN - 1932-6203
VL - 8
JO - PLoS ONE
JF - PLoS ONE
IS - 9
M1 - e76704
ER -