The ecology of Cytophaga–Flavobacteria in aquatic environments

Abstract

Culture-dependent and -independent studies have found that prokaryotic assemblages are quite diverse in aquatic habitats and contain representatives of virtually all of the roughly 40 divisions of bacteria and the major archaeal groups found so far in the biosphere [1]. Fortunately, not all of these prokaryotic groups are abundant in the plankton nor important in all biogeochemical cycles. Autotrophic and heterotrophic bacteria dominate the prokaryotic biomass in surface waters, as Archaea appear to be abundant only in the plankton of the deep oceans [2]. Among the heterotrophic bacteria, the two most abundant groups are often the Proteobacteria and the subject of this review, the Cytophaga–Flavobacteria cluster (Table 1). The relative abundance of the major heterotrophic bacterial groups in aquatic ecosystems, as determined by FISH with oligonucleotide probes The table includes only studies using probes for at least three proteobacterial subdivisions (alpha, beta and gamma) and for the Cytophaga–Flavobacteria cluster (CF). Ranges are given when the study reports several values taken over time or within a habitat. When more than depth was sampled, the surface value is reported unless noted otherwise. All DAPI-positive microbes, probably nearly all bacteria with a few Archaea and fewer (to none) Eukarya. Percent of DAPI-positive microbes that are recognized by the Eub338 probe. The relative abundance of the major heterotrophic bacterial groups in aquatic ecosystems, as determined by FISH with oligonucleotide probes The table includes only studies using probes for at least three proteobacterial subdivisions (alpha, beta and gamma) and for the Cytophaga–Flavobacteria cluster (CF). Ranges are given when the study reports several values taken over time or within a habitat. When more than depth was sampled, the surface value is reported unless noted otherwise. All DAPI-positive microbes, probably nearly all bacteria with a few Archaea and fewer (to none) Eukarya. Percent of DAPI-positive microbes that are recognized by the Eub338 probe. This paper reviews recent studies that have applied molecular methods to examine uncultured Cytophaga–Flavobacteria in freshwaters and the oceans, with the ultimate goal of using this information to better understand the role of heterotrophic bacteria in carbon cycles and other biogeochemical processes. The importance of heterotrophic bacteria in biogeochemical processes is now well appreciated, but until recently geochemists and field-orientated microbial ecologists considered these microbes as if they were a single group, even though microbiologists have been accumulating for several years information about the taxonomic and phylogenetic make up (‘community structure’) of heterotrophic bacterial communities. Only recently, however, have microbial ecologists been able to link community structure with specific biogeochemical processes (‘function’) [3]. Here I summarize briefly our progress in these areas while discussing what we know about Cytophaga–Flavobacteria in aquatic habitats. This microbial group is a natural starting point because of its high abundance in many freshwater and marine systems. The Cytophaga–Flavobacteria cluster belongs to a diverse bacterial division that has been labeled differently over the years. Hugenholtz et al. [1] and other authors have used ‘Cytophagales’ while Hamana and Nakagawa [4] recently stated that the division name was ‘Flavobacterium–Flexibacter–Bacteriodes–Cytophaga’. The latter name does give some indication of the diversity of this division and highlights some of the major genera (Fig. 1). The label used in the most recent edition of Bergey's Manual of Systematic Bacteriology [5] is simply ‘Bacteroidetes’, which will be used in this review. A more common label, however, is Cytophaga–Flavobacteria–Bacteriodes (or Flavobacterium–Bacteriodes–Cytophaga and other permutations), similar to the label (Cytophaga–Flexibacter–Bacteriodes) originally used by Woese and colleagues [6]. Other genera, which are prominent because of their association with humans, include Prevotella and Porphyromonas[7]. A phylogenetic tree of the Bacteroidetes division, illustrating the Cytophaga–Flavobacteria cluster, based on nearly complete 16S rRNA sequences. The tree was constructed using ARB and the latest data set (May 2001) available at http://www.arb-home.de/. The numbers refer to the number of strains grouped together. The Cytophaga–Flavobacteria cluster can be characterized by both phenotypic traits and 16S rRNA sequence data. As first described by Winogradsky, Cytophaga-like bacteria are unicellular, gliding, nonspore-forming Gram-negative rods, although shape can vary [8]. Colonies of many Cytophaga-like bacteria are pigmented due to flexirubin-type pigments found only in these bacteria and flavobacteria. Most notably, Cytophaga–Flavobacteria are chemoorganotrophic and are especially proficient in degrading various biopolymers such as cellulose, chitin, and