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The Genus Aquaspirillum

  • Bruno Pot
  • Monique Gillis
  • Jozef De LEY

Abstract

Helical bacteria have been found in nature under very diverse circumstances. For over 300 years people have admired these graceful forms of life under the microscope. Van Leeuwenhoek (1670) mentioned helical shapes when he described the first bacteria (animalcules). In contrast to their easy detection, spirilla have been very difficult to isolate and to maintain in pure culture. Müller (1773, 1786) described eight species of the genus Vibrio, three of which were spirilliforms. According to Williams (1959), the present type species of the genus Aquaspirillum, Aquaspirillum serpens, can be recognized in Müller’s original description of “Vibrio serpens,” but as noted by Terasaki (1980) and Krieg and Hylemon (1976), it is very unlikely that identification by modern standards can be made from the descriptions and drawings made by Müller.

The genus Spirillum was created by Ehrenberg (1832), with Spirillum volutans as the type species. Migula (1894, 1895, 1900) described many species within the genus Spirillum, mostly, however, based on mixed cultures. The genus Spirillum was reviewed thoroughly by Williams and Rittenberg (1957). They retained 19 species, mainly on the basis of morphology and a few nutritional and physiological characteristics. By cross-agglutination tests of cells of all 29 Spirillum strains, using antisera specific for Spirillum thermolabile antigens, McElroy and Krieg (1971) found 17 serogroups. Their subdivision was the basis of the classification of the genus Spirillum presented in the eighth edition of Bergey’s Manual of Determinative Bacteriology (Krieg, 1974). However, Hylemon et al. 1973 proposed that the genus Spirillum be split into the genera Aquaspirillum, Oceanospirillum, and Spirillum on the basis of DNA base composition and a limited number of physiological characteristics. Large obligately microaerophilic spirilla with large bipolar tufts of flagella and having a DNA base composition of 38 mol% GC constituted the redefined genus Spirillum (Hylemon et al., 1973), for which only one species, the type species of the original genus Spirillum (Spirillum volutans [Ehrenberg, 1832]), was described (see The Genus Spirillum in Volume 5). All marine spirilla requiring seawater for growth and having a GC content of 42 to 48 mol% were included in the new genus Oceanospirillum, containing five species (see The Genus Oceanospirillum in the second edition). Oceanospirillum was later extended with eight new species (Terasaki, 1973; Bowditch et al., 1984). The genus Aquaspirillum, with 13 species, was created for all aerobic freshwater spirilla having a low salt tolerance and a GC content of 50 to 65 mol%. Later the genus was also extended by addition of five new species (Aragno and Schlegel, 1978; Kumar et al., 1974; Maratea and Blakemore, 1981; Strength et al., 1976; Terasaki, 1973, 1979). As mentioned by Krieg (1981), this was an improvement over the previous classification, but it was still not entirely satisfactory. Indeed, on the basis of phenotypic characteristics, there seems to exist a continuum between the spirilla and a variety of other oxidative, Gram-negative bacteria, resulting in rather vague generic definitions. A vast polyphasic approach including genotypic studies was obviously needed to obtain a better insight in the relationship between these species. As a result Oceanospirillum has been redefined (Pot et al., 1989); it is described elsewhere (see The Genus Oceanospirillum in the second edition).

Results of DNA-rRNA hybridization studies (Pot et al., 1989) and 16S oligonucleotide cataloging (Woese et al., 1982, 1984b) incited us to explore further the inter- and intraspecific relationships within the genus Aquaspirillum. A very heterogeneous group of bacteria, spread over rRNA superfamilies III and IV, was found, indicating that Aquaspirillum can no longer be considered as one genus. The original genus name should be restricted to the species Aquaspirillum serpens, A. bengal, and A. fasciculus. As no definite proposals have been made yet to rename the other, misnamed, Aquaspirillum species, we will indicate their current (misnamed) status by square brackets.

All Aquaspirillum species described in Bergey’s Manual of Systematic Bacteriology (Krieg, 1984) share the following characteristics: they are all rigid helical cells, except for [A.] delicatum which is vibrioid and A. fasciculus which is a straight rod. All species so far examined by electron microscopy have a polar membrane underlying the cytoplasmic membrane. They generally have bipolar tufts of flagella, but one single flagellum at each pole may be present (as in [A.] polymorphum and A. magnetotacticum, the latter being the only named Aquaspirillum species which was not included in our taxonomic investigations; for detailed information see Blakemore et al., 1989). In addition, [A.] delicatum possesses one or two flagella at one pole only. Intracellular poly-β-hydroxybutyrate is formed (except in [A.] gracile and [A.] psychrophilum) or is presumably formed (A. magnetotacticum). Coccoid bodies which predominate in old cultures (three to four weeks) may be formed ([A.] peregrinum subsp. peregrinum, [A.] polymorphum, [A.] itersonii and A. fasciculus). Aquaspirilla are typically aerobic, although some species grow in microaerophilic conditions ([A.] peregrinum and A. fasciculus), under which these species may exhibit nitrogenase activity (Strength et al., 1976). They have a respiratory type of metabolism with oxygen as terminal electron acceptor although some species can also grow anaerobically using nitrate. They are chemoorganotrophic; however, one species ([A.] autotrophicum) is facultatively autotrophic, as it can oxidize hydrogen. Only a few species can catabolize a limited number of carbohydrates; amino acids or organic acids usually serve as the major carbon source. Since the original description, the range of GC content of the genus has been extended to vary between 49 and 66 mol%. An overview of differentiating phenotypic features is listed in Table 1.

Table 1.

Differentiating characteristics for all species presently included in the genus Aquaspirillum.

Differentiating characteristics

A. serpens a

A. bengal a

A. fasciculus a

[A.] putridiconchylium a

[A.] dispar a

[A.] autotrophicum a

[A.] aquaticum a

[A.] delicatum a

[A.] gracile a

[A.] metamorphum a

[A.] psychrophilum a

[A.] sinuosum a

[A.] giesbergeri a

[A.] anulus a

[A.] magnetotacticum b

[A.] polymorphum c

[A.] itersonii subsp. itersoniic

[A.] itersonii subsp. nipponicumd

[A.] peregrinum subsp. peregrinumc

[A.] peregrinum subsp. integrumc

Cell diameter (µm)e

0.6–1.1

0.9–1.2

0.7–0.9

0.7–1.2

0.5–0.7

0.6–0.8

0.5–0.6

0.3–0.4

0.2–0.3

0.7–1.3

0.7–0.9

0.6–0.9

0.7–1.4

0.8–1.4

0.2–0.4

0.3–0.5

0.4–0.6

0.5–0.8

0.5–0.7

0.5–0.7

Shape

H

H

SR

H

H

H

H

V

H

H

H

H

H

H

H

H

H

H

H

H

Type of helix

C

C

HA

C

C

C

C

HA

C

C

C

C

C

C

C

CC

CC

CC

CC

CC

Wavelength of helix (µm)

3.5–12.0

4.6–8.1

HA

4.5–7.0

2.0–3.5

3.0–4.0

2.0–5.0

HA

2.8–3.5

7.5–12.0

5.5–6.5

8.6–10.5

4.5–8.4

5.0–13.0

1.0–2.0

4.0–5.0

2.5–6.0

2.5–6.0

3.0–4.5

3.0–4.5

Helix diameter (µm)

1.2–4.2

1.7–2.3

HA

1.2–2.0

1.0–2.1

ND

0.8–1.0

0.4–0.7g

0.5–2.1

2.2–3.5

1.0–1.4

1.4–3.5

1.2–5.0

1.7–4.5

ND

1.0–1.5

1.0–2.2

1.0–2.2

1.4–2.0

1.4–2.2

Length of helix (µm)

3.5–42.0

5.2–22.0

3.6–43.0f

4.0–23.0

2.1–6.5

2.0–5.0

2.5–13.0

3.0–5.0g

3.5–14.0

3.5–11.0

1.5–14.0

5.0–42.0

4.0–40.0

4.0–52.0

4.0–6.0

3.5–8.4

2.0–10.0

2.0–10.0

1.5–22.0

1.5–22.0

Polar membrane present

+

+

+

+

+

ND

+

+

+

+

ND

+

+

+

ND

+

+

+

+

+

Poly-β-hydroxybutyrate formed

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

Flagellar arrangement

BT

BT

BT

BT

BT

BT

BT

U(1–2)

BT

BT

BT

BT

BT

BT

BS

BS

BT

BT

BT

BT

Coccoid bodies predominant at 3–4 weegks

+

+

+

+

+

+

Acid produced from sugarsh

+

+

+

+

+

Optimum temperature is 20°C

+

Optimum temperature is 41°C

+

Obligately microaerophilic

+

Oxidase

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

Catalase

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

Phosphatase

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

Ureasei

d

+

+

+

ND

+

+

+

+

Indole test

ND

Nitrate reduced only to nitrite

d

+

+

+

+

+

Anaerobic growth with nitrate

+

+

+

+

+

Denitrification

+

+

+

+

+

Hydrolysis of esculin

+

+

+

+

+

Growth factors required

+j

+j

ND

ND

Glutamate as sole C-source

+

+

+

+

d

+

+

ND

+

ND

+

ND

+

+

+

+

+

Histidine as sole C-source

+

ND

ND

ND

+

+

Tryptophan and glycine as sole C-source

+

ND

ND

ND

Nitrogenase activityi

+

ND

ND

ND

+

d

d

+

+

Hydrogen autotrophyi

ND

ND

ND

ND

+

ND

ND

ND

ND

ND

ND

ND

ND

ND

Temperature range for growth, °C

12–42

15–42

ND

8–40

ND

10–35

12–42

9–40

ND

3–38

2–26

9–37

9–36

3–36

ND

14–36

12–42

12–42

11–40

11–40

pH range for growth

6.0–9.0

6.0–8.4

5.5–8.5

5.5–8.5

ND

5.0–8.0

5.5–9.0

5.5–8.5

ND

6.0–9.0

5.5–9.0

6.0–9.0

6.0–9.0

6.0–8.5

ND

6.0–8.5

5.5–9.0

5.5–9.0

5.5–9.0

5.5–9.0

Growth in presence of:

1% oxgall/1% glycine/3% NaCl

+/−/−

+/−/−

+/−/−

+/−/−

+/+/−

+/−/−

+/+/−

−/−/−

+/−/−

+/−/−

ND/ND/−

+/−/−

+/−/−

−/−/−

−/+/−

+/−/−

+/−/−

ND/ND/−

+/−/−

ND/ND/−

Water-soluble brown pigment formed in the presence of:

0.1% tyrosine

+

ND

ND

+

ND

ND

0.1% tryptophan

+

ND

ND

+

ND

ND

Water-soluble yellow-green fluorescent pigment formed

d

W

+

+

d

+

ND

+

+

ND

+

ND

Alkaline reaction in litmus milk

ND

ND

ND

+

ND

Growth on:

Eosin methylene blue agar

+

ND

+

+

ND

+

+

+

ND

ND

+

+

ND

+

ND

MacConkey agar

d

ND

+

ND

+

ND

ND

+

+

ND

ND

Triple-sugar iron agar

d

+

ND

+

+

ND

+

+

+

ND

ND

+

ND

+

ND

Methyl red-Voges Proskauer broth

d

ND

ND

+

ND

+

+

ND

+

ND

+

ND

ND

Reduction of 0.3% H2SeO3

ND

ND

ND

+

ND

ND

+

d

ND

+

ND

H2S from 0.2% cysteine in PSS broth, 7 days

+

+

− or W

+

+

+

+

+

+

ND

+

d

+

ND

+

+

+

+

+

H2S from 0.01% cystein in nutrient broth, 7 days

+

ND

ND

+

ND

ND

+

ND

+

W

W

+

+

+

+

+

Deoxyribonuclease

d

+k

ND

ND

+

+

ND

+

+

ND

+

ND

ND

Ribonuclease

d

ND

+

ND

+

+

+

+

ND

+

d

ND

+

ND

ND

GC content of DNA (mo1%)

49–51

52

62–65

52

63–65

60–62

64–65

63

64–65

63

65

57–59

57–58

58–59

65

61–62

60–64

66

60–62

64

aThis taxon was found to be in rRNA superfamily III (see The Proteobacteria: Ribosomal RNA Cistron Similarities and Bacterial Taxonomy in the second edition).

bThe taxonomic status of this species was not investigated by DNA-rRNA hybridizations. For taxonomic status see Blakemore et al. (1989).

cThis taxon was found to be in rRNA superfamily IV (see The Proteobacteria: Ribosomal RNA Cistron Similarities and Bacterial Taxonomy in the second edition).

dThe taxonomic status of this species was not investigated by DNA-rRNA hybridizations. For taxonomic status see Krieg (1984).

eBy phase-contrast microscopy of 24- to 48-h-old broth cultures.

fA. fasciculus is a straight rod; the helix length refers to the length of the rod.

g[A.] delicatum is vibrioid rather than helical, thus wavelength can not be determined; the helix diameter refers to the width of the vibrio, and length of helix refers to the length of the vibrio.

hFor [A.] gracile, acid from glucose, galactose and arabinose (aerobically). For [A.] itersonii, acid from glycerol (aerobically), fructose (aerobically and anaerobically) and glucose (anaerobically only). For [A.] peregrinum, acid from fructose (aerobically and anaerobically). Peptone concentrations must be kept low (0.2% or less) in order to detect change in pH indicator. Although [A.] itersonii and [A.] peregrinum acidify sugar media anaerobically, turbid growth does not occur and the organism should be considered to have mainly a respiratory rather than fermentative type of metabolism.

iSee “Procedures for Testing Special Characters” in Krieg (1984).

j[A.] gracile requires biotin and [A.] aquaticum requires niacin.

kPositive at 37°C but not at 41°C.

Misnamed Aquaspirillum species are indicated between straight brackets.

Symbols: +, positive for all strains; −, negative for all strains; ND, not determined; H, helical (one or more complete turns or twists); V, vibrioid (less than one complete turn or twist); SR, straight rod; C, clockwise or right-handed helix (indicated by the pattern //// when focusing on the bottom of the cells); HA, helix absent; CC, counterclockwise or left-handed helix (indicated by the pattern //// when focusing on the bottom of the cells); BT, bipolar tufts; U(1–2), 1 or 2 flagella at only one pole; BS, single flagellum at each pole; W, weak reaction; d, differs among strains.

Based on Krieg (1984) and Blakemore et al. (1989).

Keywords

Isolation Medium Nitrosomonas Europaea Calcium Lactate Beta Group Calcium Malate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Bruno Pot
  • Monique Gillis
  • Jozef De LEY

There are no affiliations available

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