Reference Work Entry

The Prokaryotes

pp 549-590

The Order Cytophagales

  • Hans Reichenbach

Abstract

In the past decade much has been learnt about the order Cytophagales and about some of the organisms belonging to it, although the majority of its members are as unfamiliar as ever. On the basis of 16S rRNA studies, we can now delimit the group with some confidence and have a well-founded idea of its phylogenetic position (Paster et al., 1985; Woese et al., 1985). Accordingly, the Cytophagales appear to be distantly related to the Bacteroides group, and these two together comprise one of the main branches, perhaps a phylum, in the bacterial phylogenetic system. The substructure of the Cytophaga branch of the phylum is more difficult to evaluate. There is a main line on which we find unicellular gliders—Cytophaga (Cy.*) johnsonae, Cy. lytica, Cy. aquatilis = Flavobacterium (Fv.) aquatile, and Sporocytophaga (Sp.) myxococcoides—but at a lower level unicellular nonmotile bacteria (Fv. breve, i.e., low GC, true flavobacteria) are also found. At a still lower level, a cluster branches off which comprises the unicellular gliders—Flexibacter (Fx.) filiformis = Fx. elegans Fx el, Cy. heparina, and Taxeobacter = Myx 2105)—unicellular nongliding flavobacteria (Fv. ferugineum), but also filamentous, multicellular, gliding (Saprospira) and nonmotile bacteria (Haliscomenobacter). It is obvious from these data that our present definition of genera does not reflect the phylogenetic situation and also that the grouping in families and perhaps orders needs to be reconsidered. Before that is done, however, 16S rRNA sequences of further species should be determined.

From what has been said above it is clear that only a preliminary characterization of the order is possible at present. In this chapter, the order Cytophagales is restricted to unicellular gliding bacteria; the relevant genera are listed in Table 1. Filamentous, gliding bacteria of the genus Saprospira may or may not belong to the order, and they are sufficiently different to justify a separate treatment (see The Order Cytophagales in this Volume); contrary to earlier suggestions, these organisms are not apochlorotic cyanobacteria (Reichenbach et al., 1986). Unicellular, gliding bacteria of the genus Lysobacter have been found to be closely linked to the xanthomonads and thus belong to the gamma branch of the Proteobacteria (Woese et al., 1985); consequently they are discussed separately (see The Genus Lysobacter in Volume 6) It should be mentioned that, in the past, lysobacters have often erroneously been classified as cytophagas; this is discussed in The Genus Lysobacter in Volume 6. On the other hand, the cytophagas have been regarded as myxobacteria for some time and accordingly named; Cy. columnaris has even been classified in the myxobacterial genus Chondrococcus (now Corallococcus). However, as pointed out above, the two groups are not phylogenetically related. The nonmobile bacteria that cluster with the Cytophagales are discussed in The Genera Flavobacterium, Sphingobacterium, and Weeksella and The Genus Haliscomenobacter in this Volume).

Table 1.

Survey of the taxonomy of the order Cytophagales of the Bacteriodes-Flavobacterium-Cytophaga branch.

Order: Cytophagales

Family: Cytophagaceae

Genera: Cytophaga

Sporocytophaga

Unnamed Cytophaga-like bacteria (serveral genera)

Flexibacter

Microscilla

Flexithrix

Capnocytophaga

Taxeobacter

(Saprospira) a

aSaprospira may or may not belong to the order. It is discussed separately in The Order Cytophagales in this Volume.

The Cytophagales as outlined above are all unicellular, gliding, Gram-negative bacteria. All have rod-shaped cells, which may differ substantially in shape. They may be short or long, delicate or stout, with tapering or rounded ends (Fig. 1). Two genera exhibit a controlled and cyclic shape change: Sporocytophaga produces resting cells in the form of spherical microcysts, and some Flexibacter species alternate between very long and extremely agile thread cells and very short, almost spherical and nonmotile rod cells (Fig. 2). Many of the other species are more or less pleomorphic, with cell populations that consist of short and very long rods and chains of cells, particularly in older cultures.

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Fig. 1.

Cell shape of the Cytophagales in phase contrast. (a) A brick red, marine, agar decomposer, probably a Microscilla species, in chamber culture; the long, flexible, thread cells have tapered ends. Bar = 25 µm. (b) CLB from soil, in chamber culture, showing the typical arrangement of cells at the swarm edge. Bar = 10 µm. (c) Cytophaga lytica, a yellow, marine, agar-digesting CLB, from SP2 liquid medium. Bar = 5 µm. (d) Cytophaga succinicans, a facultatively anaerobic freshwater CLB, from AO agar. Bar = 5 µm. (e and f) Cytophaga aurantiaca type strain, a cellulose-degrading true Cytophaga, from glucose-glutamate agar. The population in (e) consists of delicate, flexible rods, which are pleomorphic with very long and with slightly swollen cells; in (f), cells from older parts of the colony begin to produce dark, lemon-shaped inflations, which later degenerate to spheroplasts. Bar = 10 µm in both pictures. (g) Flexibacter flexilis type strain, from starch agar; one of the thread cells (top edge of the photograph) shows the beginning of branching at one end. Such branching is not uncommon among the Cytophagales. Bar = 5 µm. (h) Taxeobacter species, cells in situ on water agar with a streak of living E. coli, showing a characteristic palisade pattern. Bar = 25µm.

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Fig. 2.

Cytophagales with a cyclic change in cell shape, shown in phase contrast. (a and b) Sporocytophaga myxcococcoides from a membrane of regenerated cellulose on ST6 agar; in (a), most cells are still vegetative rods, but young microcysts and intermediary stages of cell conversion can already be seen; in (b), mature, otpically refractile microcysts are present. (c to e) Flexibacter filiformis (formerly called Fx. elagans Fx el) from VY/2 agar; (c) a slide mount from the very edge of the swarm colony shows very long, delicate, flexible, and extremely agile thread cells without, or with only very few, cross walls; (d) at some distance from the edge, the thread cells have become much shorter by fragmentation; (e) finally, the cell population consists mainly of very short rods which are also clearly fatter and darker and are no longer motile. Bars = 10 µm.

The typical colonies are spreading swarms (Fig. 3). Sometimes they are filmlike and may cover the whole culture plate within a few days. In other cases, they only expand slowly or remain more or less compact. In a few instances there is also rhizoid growth. Many Cytophagales produce brightly colored colonies in shades of yellow, orange, or brick red. The yellow and orange colonies often change immediately into red, purple, or brown if covered with a 10% KOH solution. This color change is due to flexirubin-type pigments (Fig. 4), which have so far only been found in organisms of this group (including flavobacteria). The organisms belonging to the Cytophagales may be aerobic, microaerophilic, capnophilic (CO2-requiring), or facultatively anaerobic. They are all organotrophs, many of them able to degrade biomacromolecules like proteins, chitin, pectin, agar, starch, or cellulose. They are ubiquitous, are abundant, and probably play a major role in the turnover of matter in nature (e.g., Ruschke, 1968; Ruschke and Rath, 1966). Some may also be of practical interest.

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Fig. 3.

Colonies of various diverse Cytophagales. (a) Spreading colony of a CLB from soil, growing in chamber culture, dark field. Bar = 100 µm. (b) Flexibacter filiformis Fx el, swarm colony on agar plate. Bar = 3 mm. (c) CLB from soil; typical swarm colonies emerge at the side of a streak on an agar surface. Bar = 1 mm. (d and e) CLB from soil growing on two different agar media. (d) On the poorer substrate, the colonies are relatively large and show some spreading; (e) they remain small and compact on the rich medium. Bar = 1 mm in both. (f) CLB from soil, swarm colony on CY agar showing a distinct surface pattern. Bar = 1 mm. (g) Cytophaga flevensis, an agar-digesting CLB from freshwater; as a relatively rich agar substrate was used, the colonies remained rather compact. Bar = 2 mm. (h) Flexibacter filiformis Fx el, chamber culture; dense clusters of cells are sitting in conspicuous slime tracks; phase contrast. Bar = 30 µm. (i) CLB from soil, chamber culture, edge of a swarm colony with a network of slim tracks; phase contrast. Bar = 30 µm. (j and k) Cytophaga columnaris, a fish-pathogenic CLB from freshwater; swarm colonies on MYX agar (j) and AO agar (k), showing the typical growth pattern of the organism. Bar = 1 mm in both. (l to n) Taxeobacter ocellatus Tx ol (= Myx 2105): (l and m) on water agar with a streak of living E. coli, the organism typically spreads out, producing long, tendril-like strips; (m) at a higher magnification, the unusual palisadelike arrangement of the cells becomes apparent; both phase contrast; (n) after plating on CY agar, relatively compact, brick red colonies begin to spread out. Bar = 100 µm in (l), 10 µm in (m), and 2 mm in (n).

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Fig. 4.

Flexirubin-type pigments characteristic for members of the Cytophagales. (a) Cytophaga-flexirubin from CLB. (b) Chloroflexirubin from a Flexibacter species.

A few reviews on the Cytophagales and their subgroups have been published since the first edition of The Prokaryotes and can be recommended here for further information (several chapters in Bergey’s Manual of Systematic Bacteriology, vol. 3, 1989, for detailed discussions of the taxonomic problems; also, Reichenbach and Weeks, 1981; Shewan and McMeekin, 1983; and on practical aspects: Reichenbach, 1988; see also: Bernardet, 1989; Jooste, 1985; Kath, 1990).