Flavobacterium johnsoniae as a Model Organism for Characterizing Biopolymer Utilization in Oligotrophic Freshwater Environments

Abstract

Biopolymers are important substrates for heterotrophic bacteria in oligotrophic freshwater environments, but information on bacterial growth kinetics with biopolymers is scarce. The objective of this study was to characterize bacterial biopolymer utilization in these environments by assessing the growth kinetics of Flavobacterium johnsoniae strain A3, which is specialized in utilizing biopolymers at g liter ؊1 levels. Growth of strain A3 with amylopectin, xyloglucan, gelatin, maltose, or fructose at 0 to 200 g C liter ؊1 in tap water followed Monod or Teissier kinetics, whereas growth with laminarin followed Teissier kinetics. Classification of the specific affinity of strain A3 for the tested substrates resulted in the following affinity order: laminarin (7.9 ؋ 10No specific affinity could be determined for proline, but it appeared to be high. Extracellular degradation controlled growth with amylopectin, xyloglucan, or gelatin but not with laminarin, which could explain the higher affinity for laminarin. The main degradation products were oligosaccharides or oligopeptides, because only some individual monosaccharides and amino acids promoted growth. A higher yield and a lower ATP cell ؊1 level was achieved at <10 g C liter ؊1 than at >10 g C liter ؊1 with every substrate except gelatin. The high specific affinities of strain A3 for different biopolymers confirm that some representatives of the classes Cytophagia-Flavobacteria are highly adapted to growth with these compounds at g liter ؊1 levels and support the hypothesis that Cytophagia-Flavobacteria play an important role in biopolymer degradation in (ultra)oligotrophic freshwater environments.High-molecular-weight (HMW) compounds such as polysaccharides and proteins originating from phytoplankton and bacteria usually occur at concentrations in the g liter Ϫ1 range in oligotrophic aquatic environments (8,34,36,38,54). These biopolymers are considered to be important sources of carbon and energy for the heterotrophic bacteria in these ecosystems (2, 19). Low-molecular-weight (LMW) compounds (e.g., amino acids and monosaccharides) can diffuse directly into the cell, whereas biopolymers generally require extracellular enzymatic degradation and can be utilized only by bacteria that are capable of producing specific extracellular enzymes (4, 41).Representatives of the classes Cytophagia-Flavobacteria seem to play a central role in the degradation of biopolymers in marine and freshwater environments (20,24). A high abundance of Cytophagia-Flavobacteria was observed before and during phytoplankton blooms, when phytoplankton cells release large amounts of biopolymers (17,18,58). Furthermore, Cytophagia-Flavobacteria dominated the total bacterial community in culture-independent studies where natural bacterioplankton collected from aquatic environments was exposed to polymers such as starch, chitin, and bovine serum albumin (12, 39). Whole-genome sequencing of biopolymer-degrading bacterial isolates is increasingly applied to identify genes involved in biopolymer util...

Polysaccharides and Proteins Added to Flowing Drinking Water at Microgram-per-Liter Levels Promote the Formation of Biofilms Predominated by Bacteroidetes and Proteobacteria

“…These findings are consistent with previously observed differences in growth kinetics between biofouling and planktonic growth with acetate at g C liter Ϫ1 levels (46). The average ATP levels cell Ϫ1 of the attached bacteria in the blank-BF (0.10 Ϯ 0.03 fg cell Ϫ1 ) and the biofilms formed at 10 g added C liter Ϫ1 (Ն0.20 fg cell Ϫ1 ) (Table 1) exceeded the average ATP levels cell Ϫ1 reported previously for suspended bacteria in drinking water with no additions (0.017 Ϯ 0.014 and 0.018 Ϯ 0.095 fg cell Ϫ1 ) and with added carbohydrate or protein at 10 g C liter Ϫ1 (0.061 Ϯ 0.01 fg cell Ϫ1 ) (23,36). Attached bacteria thus appear to be larger than suspended bacteria.…”

“…represented Ͼ60% of the TDC demonstrates their dominance in laminarin utilization and is in line with the previously observed proficiency of Flavobacterium spp. in laminarin utilization at g C liter Ϫ1 levels in batch tests (23,61). In the second linear growth phase with laminarin, however, both the HPC and the Flavobacterium colony count decreased by a factor of 4, whereas the TDC increased by the same factor (data not shown).…”

“…in batch tests (23,24,44,45). These findings are consistent with previously observed differences in growth kinetics between biofouling and planktonic growth with acetate at g C liter Ϫ1 levels (46).…”

“…Certain planktonic freshwater representatives of the genus Flavobacterium are particularly adapted to growth with polysaccharides and proteins at a few g C liter Ϫ1 in batch tests (23)(24)(25). However, under the turbulent flow conditions prevailing in drinking water distribution systems and in certain natural lotic freshwater systems (e.g., brooks and streams), surface-attached rather than planktonic microorganisms predominate (26).…”

Complete Genome Sequence of Flavobacterium indicum GPSTA100-9T, Isolated from Warm Spring Water

“…We determined the whole genome sequence of the type strain of Flavobacterium indicum (CIP 109464 T ) (11) in order to perform comparative genomic studies between this environmental species and other Flavobacterium species whose genome sequences have been published: two fish-pathogenic species that severely impact aquaculture worldwide (1) (F. psychrophilum JIP02/86 [4] and F. branchiophilum FL15 [13]) and another environmental species, F. johnsoniae UW101 T (7), a model organism for characterizing gliding motility (8) and biopolymer utilization in oligotrophic environments (10).…”