ELSEVIER
MICROBIOLOGY
REVIEWS
FEMS Microbiology Reviews 18 (1996) 149-158
Hyperthermophilic procaryotes
Karl O. Stetter *
Lehrstuhl ftir Mikrobiologie und Archaeenzentrum, Universit~it Regensburg, 93053 Regensburg, Germany
Abstract
Hyperthermophilic Archaea and Bacteria with optimal growth temperatures between 80°C and 110°C have been isolated
from geothermal and hydrothermal environments. By 16S rRNA sequence comparisons, they exhibit a great phylogenetic
diversity indicated by 25 different genera. Hyperthermophiles consist of anaerobic and aerobic chemolithoautotrophs and
heterotrophs growing at neutral or acidic pH. Based on their outstanding heat resistance they are interesting objects the same
for basic research as for biotechnology.
Keywords: Archaea; Hyperthermophilic; Phylogeny; Volcanism
Contents
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
150
2. Environments and enrichment of hyperthermophiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
150
3. Phylogeny of hyperthermophiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
150
4. Taxonomy of byperthermophiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
150
5. Physiological properties of byl~rthermophiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5. I. Extreme acidophiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2. Neutrophiles and moderate acidophiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
150
151
153
6. Conclusions and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
155
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
156
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
156
* Tel.: +49 (941) 943 3160; Fax: +49 (941) 943 2403; e-mail: [email protected]
0168-6445/96/$32.00 © 1996 Federation of European Microbiological Societies. All rights reserved
PII S01 6 8 - 6 4 4 5 ( 9 6 ) 0 0 0 0 8 - 3
150
K. O. Stetter / FEMS Microbiology Ret:iews 18 (1996) 149-158
1. Introduction
3. Phylogeny of hyperthermophiles
Hyperthermophilic Bacteria and Archaea
(former: archaebacteria) represent the organisms at
the upper temperature border of life [1-3]. Hyperthermophiles belong to phylogenetically distant
groups and may represent rather ancient adaptations
to heat. As a rule, they grow fastest between 80°C
and 100°C. In contrast to usual thermophiles, hyperthermophiles are unable to grow below 60°C. The
most extreme hyperthermophiles known are so well
adapted to the high temperatures that they do not
even grow at 80°C or below [4,5].
A 16S rRNA-based universal phylogenetic tree is
available, now [11,12]. It shows a tripartite division
of the living world consisting of the domains Bacteria, Archaea and Euca~a (Fig. 1). The Archaea
consist of two major kingdoms: The Crenarchaeota
(Sulfolobales-Thermoproteales branch) and the Euryarchaeota (Extreme Halophiles-Methanogens
branch). Short phylogenetic branches indicate a rather
slow clock of evolution. Deep branching points are
evidence for early separation of two groups. The
separation of the Bacteria from the Eucao'a-Archaea
lineage is the deepest and earliest branching point
known so far. Hyperthermophiles are represented
among all the deepest and shortest lineages, including Aquifex and Thermotoga within the Bacteria;
2. Environments and enrichment of hyperthermophiles
Hyperthermophiles have been isolated almost exclusively from environments with in situ temperatures between about 80 and 115°C. Biotopes of
hyperthermophiles are water-containing volcanic areas like terrestrial solfataric fields and hot springs,
shallow submarine hydrothermal systems and abyssal
hot vent systems ('Black Smokers'). Man--made
high-temperature biotopes are smoldering coal refuse
piles and geothermal power plants [6,7]. Further
communities of hyperthermophiles had been discovered recently within oil-bearing deep geothermally
heated soils [8]. Due to the low solubility of oxygen
at high temperatures and the presence of reducing
gasses, biotopes of hyperthermophiles are essentially
unoxic. However, air-exposed surfaces of solfataric
fields may contain reasonable amounts of oxygen.
Although unable to grow, hyperthermophiles may
survive for long times at ambient temperature. This
ability may be essential for spreading out through the
cold atmosphere and hydrosphere. In agreement with
this result, viable hyperthermophiles could be isolated from cold Beaufort Sea water and Pacific water
neighboring active Macdonald Sea Mount [8,9]. To
cultivate hyperthermophiles, aerobic and anaerobic
samples can to be taken from hot water, sediments
and rocks. In the laboratory, aerobic and anaerobic
enrichment cultures on various substrates are be
obtained at conditions corresponding to the original
environment. To clone hyperthermophilic enrichment
cultures, direct cloning of single cells by 'optical
tweezers' has been successfully applied now [10].
Pyrodictium, Pyrobaculum, Desulfurococcus, Sulfolobus, Methanopyrus, Thermococcus, Methanothermus, Archaeoglobus within the Archaea (Fig. 1,
bold lines). Based on these observations, hyperthermophiles may still be rather primitive and the last
common ancestor may have been a hyperthermophile
[13].
4. Taxonomy of hyperthermophiles
So far, 54 species of hyperthermophilic Bacteria
and Archaea are known (Table 1). They are divergent by their phylogeny and physiological properties
and are grouped into 25 genera and 11 orders. Within
the Bacteria, Aqu(fex pyrophilus and Thermotoga
maritima exhibit the highest growth temperatures
with 95°C and 90°C, respectively (Table 1). Within
the Archaea, the organisms with the highest growth
temperatures (between 103°C and 110°C) are members of the genera Pyrobaculum, Pyrodictium, Pyrococcus and Methanopyrus.
5. Physiological properties of hyperthermophiles
Hyperthermophiles are well adapted to their
biotopes, being able to grow at high temperatures
and extremes of pH, redox potential and salinity
(Table 1). Within their habitats, hyperthermophiles
form complex ecosystems consisting of a variety of
K.O. Stetter/ FEMS Microbiology Ret,iews 18 (1996) 149-158
primary producers and decomposers of organic matter. Primary producers are chemolitboautotrophs using inorganic electron donors and acceptors in their
energy-yielding reactions (Table 2).
5.1. Extreme acidophiles
Members of extremely acidophilic hyperthermophiles, including the genera Sulfolobus, Metallosphaera (Fig. 2c), Acid|anus and S~giolobus, are
found in terrestrial and marine solfataric fields and
smoldering coal refuse piles, e.g. [1,3,7,14]. They
grow aerobically, facultatively aerobically or strictly
anaerobically at acidic pH (opt. about pH 3). Members of Sulfolobus are strict aerobes growing au-
totrophically by oxidation of S °, S 2 and H e, forming sulfuric acid or water as end product (Tables 2
and 3). Sulfolobus brierleyi (now renamed: Acid|anus brierlevi) and Sulfolobus metallicus are able to
grow by leaching of sulfidic ores [15,16]. Several
Su![olobus isolates are facultative or obligate heterotrophs, growing on sugars, yeast extract and peptone [14]. Under microaerobic conditions, Su!folobus
isolates are able to reduce ferric iron and molybdate
[17]. Growth of SulJblobus requires low ionic
strength. In agreement, Su!folobus was not found in
marine solfataric fields. Metallosphaera sedula.
which differs from Suifolobus species by the much
higher GC-content of its DNA ('Fable 3), is a powerful oxidizer of sulfidic ores like pyrite, chalcopyrite
Eucarya
marl
animals
microsporidia
flagellates
plants
dipiomonads
green
non-sulfur
bacteria
Bacteria
Archaea
Su|folobus
gram positives
proteobactena
I
Desulfuroeoccus
Thermotoga
T~rmopmteus
tlavobacteria
Pyrobaculum
) PyI'ococcus
Mcthanobactenum
wArchaeoglobus
~
Aquifex
151
3 '
~'-~,.,Halo~cterium
4
~
Methanoplanus
M©thanococcus
k Methanospinllum
1 jamasaxii
2 iga~s
Methanosarcina
3 ammalitlaotzel~eas
4 vmmcllii
Fig. 1. Hyperthermophiles within the phylogenetic tree: schematically redrawn and modified from [12].
152
K.O. Stetter / FEMS Microbiology Rec~iews 18 (1996) 149-158
Table 1
Taxonomy and upper growth temperatures of hyperthermophiles
Order
Genus
Species
BACTERIA
Thermotogales
Thermotoga
T. maritima
T. neapolitana
T. thermarum
T. elfii
T. africanus
F. nodosum
F. islandicum
G. petrea
G. subterranea
P. miotherma
A. pyrophilus
Thermosipho
Fervidobacterium
Geotoga
Aquificiales
Petroga
Aquifex
ARCHAEA
Sulfolobales
Sulfolobus
Metallosphaera
Acidianus
Thermoproteales
Desulfurolobus
Stygiolobus
Thermoproteus
Pyrobaculum
Thermofilum
Desulfurococcales
Desulfurococcus
Pyrodictiales
Staphylothermus
Pyrodictium
Thermococcales
Hyperthermus
Thermodiscus
Thermococcus
Pyrococcus
Archaeoglobales
Archaeoglobus
Methanobacteriales
Methanothermus
S. acidocaldarius
S. solfataricus
S. shibatae
S. metallicus
M. sedula
A. infernus
A. brierleyi
D. ambivalens
S. azoricus
T. tenax
T. neutrophilus
T. uzoniensis
P. islandicum
P. organotrophum
P. aerophilum
T. pendens
T. librum
D. mobilis
D. mucosus
D. saccharovorans
D. amylolyticus
S. marinus
P. occulmm
P. brockii
P. abyssi
H. butylicus
T. maritimus
T. celer
T. litoralis
T. stetteri
T. profundus
T. alcaliphilus
7: chitonophagus
P. furiosus
P. woesii
A. fulgidus
A. profundus
M. fervidus
M. sociabilis
Tmax(°C)
90
90
84
72
77
80
80
55
60
65
95
*
*
*
*
*
*
*
85
87
86
75 ~
80 *
95
75 *
95
89
97
97
97
103
103
104
95
95
95
97
97
97
98
110
110
110
108
98
93
98
98
90
90
93
103
103
92
92
97
97
Ref.
[27]
[33]
[34]
[35]
[36]
[37]
[38]
[39]
[39]
[39]
[29]
[40]
[41]
[42]
[ 16]
[43]
[19]
[ 15]
[44]
[20]
[45]
[46]
[47]
[48]
[48]
[21 ]
[49]
[46]
[50]
[50]
[46]
[51]
[52]
[53]
[53]
[54]
[55]
[46]
[56]
[57]
[58]
[59]
[24]
[25]
[22]
[60]
[61 ]
[62]
[63]
[64]
K.O. Stetter / FEMS Microbiology Reviews 18 (1996) 149-158
153
Table 1 (continued)
Order
Genus
Species
Tmax(°C)
Ref.
Methanococcales
Methanococcus
Methanopyrales
Methanopyrus
M. thermolithotrophicus
M. jannaschii
M. igneus
M. kandleri
70 *
86
91
110
[65]
[66]
[67]
[30]
• Moderate therrnophiles related to hyperthermophiles.
and sphalerite, forming sulfuric acid and solubilizing
heavy metal ions (Table 2). Acidianus similar to
Sulfolobus is able to grow by oxidation of S °, sulfides, H 2 and organic matter. In addition, it is able to
grow anaerobically by reduction of elemental sulfur
with H 2 as electron donor [18]. Members of Acidianus are able to grow in the presence of up to 4%
salt and have been isolated from a marine hydrotherreal system [19]. Stygiolobus is a strictly anaerobic
extreme acidophile, growing obligately chemolithoautotrophically by reduction of S o with H 2 [20].
5.2. Neutrophiles and moderate acidophiles
Communities of neutrophilic and slightly acidophilic hyperthermophiles are found in terrestrial
solfataric fields, submarine hydrothermal systems and
deep oil reservoirs [8]. Most of them are strict anaerobes. Terrestrial solfataric fields contain members of
the genera Thermoproteus, Pyrobaculum, Thermofilum, Desulfurococcus and Methanothermus
(Tables 2 and 3). Cells of members of Thermoproteus, Pyrobaculum and Thermofilum are almost rectangular rods. During the exponential growth phase,
spheres are visible at the ends ('golf clubs'). Cells of
Thermofilum are only about 0.17 to 0.35 /xm in
diameter, while those of Pyrobaculum and Thermoproteus are about 0.50 /zm. Thermoproteus neu-
trophilus, Thermoproteus tenax and Pyrobaculum
islandicum are able to grow chemolithoautotrophically by anaerobic reduction of S O by H 2 (Table 2).
As an exception, Pyrobaculum aerophilum is a marine organism able to grow anaerobically by reduction of nitrate by H 2 and on H 2 and 02 under
microaerobic conditions [21]. Strains of Pyrobaculure organotrophum, Thermoproteus uzoniensis and
Thermofilum are obligate heterotrophs growing on
organic substrates by sulfur respiration. Thermoproteus tenax and Pyrobaculum islandicum are facultative heterotrophic sulfur respirers. Members of
Desulfurococcus, Staphylothermus and Thermodiscus are coccoid and disk-shaped strictly heterotrophic sulfur respirers. Members of Thermococcus and Pyrococcus gain energy by fermentation of
peptides, amino acids and sugars, forming fatty acids,
CO 2 and H 2. Hydrogen is inhibitory to growth and
can be removed by gassing with N 2 [22]. Alternatively, hydrogen inhibition can be prevented by the
addition of S °, where upon H2S is formed instead of
H 2. Pyrococcusfuriosus is able to ferment pyruvate,
forming acetate, H 2 and CO 2 [23]. Pyrococcus and
Thermococcus species were found in oil reservoirs,
too [8]. Thermococcus alcaliphilus (Fig. 2b) is able
to grow up to pH 10.5, while Thermococcus
chitonophagus represents a novel hyperthermophilic
chitin degrader [24,25]. Many terrestrial and subma-
Table 2
Energy-yielding reactions in chemolithoautotrophic hyperthermophiles
Energy-yielding reaction
Genera
4H 2 + CO 2 ~ CH 4 4- 2 H 2 0
H 2 + S ° ~ H2S
4H 2 + H2SO 4 ~ H2S + 4 H z O
H 2 + H N O 3 ~ HNO 2 + H 2 0
H 2 + 1/202 ~ H20
2S ° + 302 + 2 H 2 0 ~ 2 H 2 S O 4
(FeS 2 + 702 + 2 H 2 0 ~ 2FeSO 4 + 2 H 2 S O 4)
Methanopyrus, Methanothermus, Methanococcus
Pyrodictium, Thermoproteus, Pyrobaculum, Acidianus, So'giolobus
Archaeoglobus
Pyrobaculum, Aquifex
Pyrobaculum, Aquifex, Sulfolobus, Acidianus, Metallosphaera
Aqulfex, Sulfolobus, Acidianus, Metallosphaera
154
K.O. Stetter/ FEMS Microbiology Ret,iews 18 (1996) 149-158
rine hydrothermal fields contain members of the
bacterial genus Thermotoga which are rod-shaped
cells surrounded by a characteristic sheath-like structure ('Toga') overballooning at the ends (Table 3).
The Toga contains porins and is most likely homologous to the outer membrane of gram-negative bacteria [26]. Thermotoga ferments various carbohydrates
like glucose, starch and xylanes, forming acetate,
L-lactate, H 2 and CO 2 as end products [27]. The
rod-shaped (Fig. 2a) chemolithoautotrophic Aquifex
pyrophilus represents the deepest phylogenetic
branch within the bacterial domain [28] (Fig. 1).
Aquifex gains energy by oxidation of hydrogen or
sulfur under microaerobic conditions [29]. Alternatively, Aquifex is able to use nitrate as electron
acceptor (Table 2). Archaeal coccoid sulfate reducers
are members of Archaeoglobus. Some species occur
within hot oil reservoirs and may be responsible for
Fig. 2. Electron micrographs of hyperthermophilic microorganisms(bar, 0.5 /xm) Preparation: a-c: freeze etching; d: scanning electron
micrograph a Aquifex pyrophilus b Thermococcus alcaliphilus c Metallo6phaera sedula d Pyrodictium abyssi.
K.O. Stetter / FEMS Microbiology Reviews 18 (1996) 149-158
155
members of Archaea, Methanopyrus species contain
2,3-di-O-geranylgeranyl-sn-glycerol as the dominating membrane lipid [31]. Further marine
methanogenic hyperthermophiles are Methanococcus
igneus and Methanococcus jannaschii (Table 1).
H2S production, there ('reservoir souring') [8]. In
the laboratory, growth is stimulated by crude oil.
Archaeoglobus fulgidus and Archaeoglobus lithotrophicus are able to gain energy by reduction of
SO 4- by H 2. Archaeoglobus profundus is an obligate heterotroph. Archaeoglobus fulgidus possesses
several coenzymes which had been assumed to be
unique for methanogens. The organisms with the
highest growth temperature are members of Pyrodictium and Methanopyrus, growing at ! 10°C. Cells of
Pyrodictium are disk-shaped and are connected by a
network of ultrathin hollow tubules (Fig. 2d). Strains
of Pyrodictium are usually chemolithoantotrophs
gaining energy by reduction of S O by H~. Pyrodictium abyssi is a heterotroph growing by peptide
fermentation. Methanopyrus kandleri is a rod-shaped
methanogen with a pseudomurein cell wall covered
by an S-layer. Representing the deepest and shortest
phylogenetic branch within the Archaea (Fig. 1),
members of Methanopyrus are strict chemolithoautotrophs that grow optimally at 100°C with a doubling time of 50 min [5,30]. In contrast to all other
6. Conclusions and perspectives
There is an unanticipated diversity of species of
hyperthermophiles within high temperature environments. It is evident by 16S rRNA diversity and by
unusual physiologic properties. In their biotopes,
hyperthermophiles are either primary producers or
consumers of organic matter. Energy conservation in
primary producers occurs by anaerobic and aerobic
types of respiration, in which molecular hydrogen is
mainly used as an electron donor. Consumers gain
energy either by anaerobic or aerobic types of respiration or by fermentation.
Direct microscopic inspection of hot biotopes indicates there are many other morphotypes yet to be
Table 3
Growth conditions and morphological and biochemical features of hyperthermophiles
Species
Growth conditions
Temperature (°C)
Sulfolobus acidocaldarius
Metallosphaera sedula
Acidianus infernus
St3'giolobus azoricus
Thermoproteus tenazc
Pvrobaculum islandicum
Pyrobaculum aernphilum
Thermofilum pendens
Desulfurococcus mobilis
Staphylothermus marinus
Pyrodictium occultum
Thermodiscus maritimus
Thermococcus celer
Thermococcus alcaliphilus
Pyrococcus.furiosus
Archaeoglobusfulgidus
Methanothermus sociabilis
Methanopyrus kandleri
Methanococcus igneus
Thermotoga maritima
Aquifex pyrophilus
pH
Minimum
Optimum
Maximum
60
50
60
57
70
74
75
70
70
65
82
75
75
56
70
60
65
84
45
55
67
75
75
88
80
88
100
100
88
85
92
105
88
87
85
100
83
88
98
88
80
85
80
80
95
89
97
103
104
95
95
98
110
98
93
90
105
95
97
110
91
90
95
marine (m); terrestrial (t).
Habitat *
DNAmol%
G+C
Morphology
37
45
31
38
56
46
52
57
51
35
62
49
57
43
38
46
33
60
31
46
40
lobed cocci
cocci
lobed cocci
lobed cocci
regular rods
regular rods
regular rods
slender regular rods
cocci
cocci in aggregates
discs with fibres
discs
cocci
cocci
cocci
irregular cocci
rods in clusters
rods in chains
irregular cocci
rods v, ith sheath
rods
Aerobic (ae)
Anaerobic (an)
1-5
ae
t
1-4.5
ae
t
ae/an
t
an
t
an
t
an
t
1.5-5
1-5.5
2.5-6
5-7
5.8--9
4-6.5
4.5-7
4.5-8.5
5-7
5-7
4-7
6.5-10.5
5-9
5.5-7.5
5.5-7.5
5.5 -7
5-7.5
5.5-9
5.4-7.5
ae/an
m
an
t
an
t
an
m
an
an
an
an
an
an
an
an
an
an
ae
m
m
m
m
in
m
t
m
in
m
m
156
K. O. Stetter / FEMS Microbiology Reciews 18 (1996) 149-158
cultivated. Moreover, extraction and amplification of
DNA corresponding to 16S rRNA from a hot spring
indicates the presence of many unknown members of
Archaea [32]. Since cultivation is the prerequisite for
understanding how hyperthermophiles live and which
roles they play within high temperature ecosystems,
learning how to cultivate them is a critical challenge
in the future.
[11]
[12]
[13]
Acknowledgements
[14]
I wish to thank Gertraud Rieger for the preparation of the electron micrographs. The work presented
from my laboratory was supported by grants of the
Deutsche Forschungsgemeinschaft, the Bundesministerium f'tir Forschung und Technologic and the Fonds
der Chemischen Industrie.
[15]
[16]
[17]
References
[18]
[1] Brock, T.D. (1986) Thermophiles: General, Molecular and
Applied Microbiology. John Wiley & Sons, New York.
[2] Stetter, K.O. and Zillig, W. (1985) Thermoplasma and the
thermophilic sulfur-dependent archaebacteria. In: The Bacteria (Wolfe, R.S. and Woese, C.R., Eds.), Vol. 8, pp. 85-170.
Academic Press, New York.
[3] Stetter, K.O. (1992) Life at the upper temperature border. In:
Frontiers of Life (Tran Thanh Van, J., Tran Than Van, K.,
Mounolou, J.C., Schneider. J. and McKay, C., Eds.), pp.
195-219. Gifsur-Yvette: Editions Fronti~res.
[4] Stetter, K.O. (1982) Ultrathin mycelia-forming organisms
from submarine volcanic areas having an optimum growth
temperature of 105°C. Nature 300, 258-260.
[5l Huber, R., Kurr, M., Jannasch, H.W. and Stetter, K.O.
(1989) A novel group of abyssal methanogenic archaebacteria (Methanopyrus) growing at 110°C. Nature 342, 833-834.
[6] Marsh, R.M. and Norris, P.R. (1985) The isolation of some
thermophilic, autotrophic iron- and sulfur-oxidizing bacteria.
FEMS Microbiol. Lett. 17, 311-315.
[7] Fuchs, T.M. (1994) Physiologische und molekularbiologische
Untersuchungen an neu isolierten thermoacidophilen Archaeen. Diplomarbeit, Universi~t Regensburg, Germany.
[8] Stetter, K.O., Huber, R., Bl~Schl, E., Kurr, M., Eden, R.D.,
Fiedler, M., Cash, H. and Vance, I. (1993) Hyperthermophilic archaea are thriving in deep North Sea and Alaskan
oil reservoirs. Nature 300, 743-745.
[9] Huber, R., Stoffers, P., Cheminee, J.L., Richnow, H.H. and
Stetter, K.O. (1990) Hyperthermophilic archaebacteria within
the crater and open-sea plume of erupting Macdonald
Seamount. Nature 345, 179-182.
[10] Huber, R., Burggraf, S., Mayer, T., Barns, S.M., Rognagel,
[19]
[20]
[21]
[22]
[23]
[24]
[25]
P. and Stetter, K.O. (1995) Isolation of a hyperthermophilic
archaeum predicted by in situ RNA analysis. Nature 376,
57-58,
Woese, C.R. and Fox, G.E. (1977) Phylogenic structure of
the prokaryotic domain: the primary kingdoms. Proc. Natl.
Acad. Sci. USA 74, 5088-5090.
Woese, C.R., Kandler, O. and Wheelis, M.L. (1990) Towards
a natural system of organisms. Proposal for the domains
Archaea, Bacteria and Eucao'a. Proc. Natl. Acad. Sci. USA
87, 4576-4579.
Stetter, K.O. (1994) The lesson of Archaebacteria. In: Nobel
symposium (Bengtson, S., Ed.), No. 84, pp. 143-151,
Columbia University Press, New York.
Brock, T.D. (1978) Therrnophilic Microorganisms and Life
at High Temperatures. Springer-Verlag, New York.
Brierley, C.L. and Brierley, J.A. (1973) A chemolithoautotrophic and thermophilic microorganism isolated from an
acidic hot spring. Can. J. Microbiol. 19, 193-198.
Huber, G. and Stetter, K.O. (1991) Sulfolobus metallieus, sp.
nov., a novel strictly chemolithoantotrophic thermophilic archaeal species of metal mobilizers. System. Appl. Microbiol.
14, 372-378.
Brierley, C.L. and Brierley, J.A. (1982) Anaerobic reduction
of Sulfolobus species. Zentralblatt f. Bakteriologie und Hygiene, I. Abteilung Originale C 3, 289-294.
Segerer, A., Stetter, K.O. and Klink, F. (1985) Two contrary
modes of chemolithoautotrophy in the same archaebacterium.
Nature 313, 787-789.
Segerer, A., Neuner, A., Kristjansson, J.K. and Stetter, K.O.
(1986) Acidianus infernus gen. nov., sp. nov., and Acidianus brierleyi comb. nov.: Facultatively aerobic, extremely
acidophilic thermophilic sulfur-metabolizing archaebacteria.
J. Bacteriol. 36, 559-564.
Segerer, A.H., Trincone, A., Gahrtz, M. and Stetter, K.O.
(1991) Stygiolobus azoricus gen. and sp. nov., represents a
novel genus of anaerobic, extremely thermoacidophilic archaea of the order Sulfolobales. J. Bacteriol. 41,495-501.
V~ilkl, P., Huber, R., Drobner, E., Rachel, R., Burggraf, S.,
Trincone, A. and Stetter, K.O. (1993) Pyrobaculum
aerophilum sp. nov., a novel nitrate-reducing hyperthermophilic archaeum. Appl. Environ. Microbiol. 59, 29182926
Fiala, G. and Stetter, K.O. (1986) Pyrococcus furiosus sp.
nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch. Microbiol. 145,
56-61.
Schafer, T. and SchiSnheit, P. (1992) Maltose fermentation to
acetate, CO z and H 2 in the anaerobic hyperthermophilic
archaeon Pyrococcusfuriosus: evidence for the operation of
a novel sugar fermentation pathway. Arch. Microbiol. 158,
188-202.
Keller, M., Braun, F.-J., Dirmeier, R., Hafenbradl, D.,
Burggraf, S., Rachel, R. and Stetter, K.O. (1995) Thermococcus alcaliphilus sp. nov., a new hyperthermophilic archaeum growing on polysulfide at alkaline pH. Arch. Microbiol. 164, 390-395.
I-Iuber, R., St~Shr, J., Hohenhaus, S., Rachel, R., Burggraf,
K.O. Stetter / FEMS Microbiology Ret;iews 18 (1996) 149-158
[26]
[27]
[28]
[29]
[30]
[31]
[32]
[33]
[34]
[35]
[36]
[37]
Jannasch, H.W. and Stetter, K.O. (1995) Thermococcus
chitonophagus sp. nov., a novel, chitin-degrading, hyperthermophilic archaeum from a deep-sea hydrothermal vent environment. Arch. Microbiol. 164, 255-264.
Rachel, R., Engel, A.M. Huber, R., Stetter, K.O. and
Baumeister, W. (1990) A porin-type protein is the main
constituent of the cell envelope of the ancestral eubacterium
Thermotoga maritima. FEBS Lett. 262, 64-68.
Huber, R., Langworthy, T.A., K~Snig,H., Thomm, M., Woese,
C.R., Sleytr., U.B. and Stetter, K.O. (1986) Thermotoga
maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90°C. Arch.
Microbiol. 144, 324-333.
Burggraf, S., Olsen, G.J., Stetter, K.O. and Woese, C.R.
(1992) A phylogenetic analysis of Aquifex pyrophilus. System. Appl. Microbiol. 15, 352-356.
Huber, R., Wilharm, T., Huber, D., Trincone, A., Burggraf,
S., Ktinig, H., Rachel, R., Rockinger, I., Fricke, H. and
Stetter, K.O. (1992) Aquifex pyrophilus gen. nov. sp. nov.,
represents a novel group of marine hyperthermophilic hydrogen-oxidizing bacteria. System. Appl. Microbiol. 15, 340351.
Kurr, M., Huber, R., KSnig, H., Jannasch, H.W., Fricke, H.,
Trincone, A., Kristjansson, J.K. and Stetter, K.O. (1991)
Methanopyrus kandleri gen. and sp. nov., represents a novel
group of hyperthermophilic methanogens, growing at 110°C.
Arch. Microbiol. 156, 239-247.
Hafenbradl, D., Keller, M. Thiericke, R. and Stetter, K.O.
(1993) A novel unsaturated archaeal ether core lipid from the
hyperthermophile Methanopyrus kandleri. System. Appl Microbiol. 16, 165-169.
Barns, S.M., Fundyga, R.E., Jeffries, M.W. and Pace, N.R.
(1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc. Natl.
Acad. Sci. USA 91, 1609-1613.
Jannasch, H.W., Huber, R., Belkin, S. and Stetter, K.O.
(1988) Therrnotoga neapolitana, sp. nov. of the extremely
thermophilic, eubacterial genus Thermotoga. Arch. Microbiol. 150, 103-104.
Windberger, E., Huber, R., Trincone, A., Fricke, H. and
Stetter, K.O. (1989) Therrnotoga thermarum sp. nov. and
Thermotoga nectpolitana occuring in African continental solfataric springs. Arch. Microbiol. 151, 506-512.
Ravot, G., Magot, M., Fardeau, M.-L., Patel, B.K.C., Prensier, G., Egan, A., Garcia, J.-L. and Ollivier, B. (1995)
Thermotoga elfii sp. nov., a novel thermophile bacterium
from an African oil-producing well. Int. J. Syst. Bacteriol.
45(2), 308-314.
Huber, R., Woese, C.R, Langworthy, T.A., Fricke, H. and
Stetter, K.O. (1989) Thermosipho africanus gen. nov., represents a new genus of thermophilic eubacteria within the
'Thermogales'. System. Appl. Microbiol. 12, 32-37.
Patel, B.K.C., Morgan, H.W. and Daniel, R.M. (1985) FerL,idobacterium nodosum gen. nov. and spec. nov., a new
chemoorganotrophic, caldoactive, anaerobic bacterium. Arch.
Microbiol. 141, 63-69.
157
[38] Huber, R., Woese, C.R., Langworthy, T.A., Kristjansson,
J.K. and Stetter, K.O. (1990) Fervidobacterium islandicum
sp. nov., a new extremely thermophilic eubacterium belonging to the 'Thermotogales'. Arch. Microbiol. 154, 105-111.
[39] Davey, M.E., Wood, W.A., Key, R., Nakamura, K. and
Stahl, D. (1993) Isolation of three species of Geotoga and
Petrotoga: two new genera, representing a new lineage in the
bacterial line of descent distantly related to the 'Thermotogales'. System. Appl. Microbiol. 16, 191-20(I.
[40] Brock, T.D., Brock, K.M,, Belly, R.T. and Weiss, R.L.
(1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria
living at low pH and high temperature. Arch. Microbiol. 84,
54-68.
[41] Zillig, W., Stetter, K.O., Wunderl, S., Schulz, W., Priess, H.
and Scholz, I. (1980) The Sulfolobus-Caldariella group:
taxonomy on the basis of the structure of DNA-dependent
RNA polymerases. Arch. Microbiol. 125, 259-269.
[42] Grogan, D., Palm, P. and Zillig, W. (1990) Isolate B 12,
which harbours a virus-like element, represents a new species
of the archaebacterial genus Sulfolobus, Solfolobus shibatae,
sp. nov. Arch. Microbiol. 154, 594-599.
[43] Huber, G., Spinnler, C., Gambacorta, A. and Stetter, K.O.
(1989) Metallo.~phaera sedula gen. and sp. nov., represents a
new genus of aerobic, metal-mobilizing, thennoacidophilic
archeabacteria. System. Appl. Microbiol. 12, 38-47.
[44] Zillig, W., Yeates, S., Holz, I., BiSck, A., Gropp, F. and
Simon, G. (1987) Desulfurolobus ambiL'alens, gen. nov. sp.
nov., an autotrophic archaebacterium facultatively oxidizing
or reducing sulfur. System. Appl. Microbiol. 8, 197-203.
[45] Zillig, W., Stetter, K.O., Sch~ifer, W., Janecovic, D., Wunderl, S., Holz, I. and Palm, P. (1981) Thermoproteales: a
novel type of extremely thermoacidophilic anaerobic archaebacteria isolated from Icelandic solfataras. Zentralblatt ftir
Bakteriologie und Hygiene, I. Abteilung Originale C2, 205227.
[46] Stetter, K.O. (1986) Diversity of extremely thermophilic
archaebacteria. In: Thermophiles: General, Molecular and
Applied Microbiology (Brock, T.D., Ed.), pp. 40-74. John
Wiley & Sons, New York.
[47] Bonch-Osmolovskaya, E.A., Miroshnichenko, M.L., Kostrikina, N.A., Chernych, N.A. and Zavarzin, G.A. (1990) Thermoproteus uzoniensis sp. nov., a new extremely thermophilic
archaebacterium from Kamchatka continental hot springs,
Arch. Microbiol. 154, 556-559.
[48] Huber, R., Kristjansson, J.K. and Stetter, K.O. (1987) Pyrobaculum gen. nov. a new genus of neutrophilic, rod-shaped
archaebacteria from continental solfataras growing optimally
at 100°C. Arch. Microbiol. 149, 95-101.
[49] Zillig, W., Gierl, A., Schreiber, G., Wunderl, S., Janecovic,
D., Stetter, K.O. and Klenk, H.P. (1983) The archaebacterium Thermofilum pendens represents, a novel genus of
thermophilic, anaerobic sulfur-respiring Thermoproteales.
System. Appl. Microbiol. 4, 79-87.
[50] Zillig, W., Stetter, K.O., Prangishvilli, C., Sch~ifer, W., Wunderl, S., Janecovic, D., Holz, I. and Palm, P. (1982) Desulfurococcaceae, the second family of the extremely ther-
K.O. Stetter / FEMS Microbiology Reviews 18 (1996) 149-158
158
rnophilic, anaerobic, sulfur-respiring Thermoproteales. Zentralblatt ftir Bakteriologie mad Hygiene, I. Abteilung Originale C 3, 304-317.
[51] Boach-O~molovskaya, E.A., ~ e v ,
A.I., Miroshnichenko,
M.L., Svetlichnaya, T.P. and Alexeyev, V.A. (1985) Characteristics of Desulfurococcus amylolyticus n. sp., a new extreme thermophilic archaebactr,xium from hot volcanic vents
of Karnchatlo and Ktmashir. Microbiologyia 57, 78-85 (in
Russian)
[52] Fiala, G., Slitter, K.O., .lannasch, H.W., Langworthy, T.A.
and Madon, J. (1986) Staphylothermus marinus sp. nov.
represents a novel genus of extremely thermophilic submarine heterotrophic archaebacteria growing up to 98°C. System. Appl. Microbiol. 8, 106-113.
[53] Stetter, K.O., K~inig, H. and Stackebrandt, E. (1983) Pyrodictium gen. nov., a new genus of submarine disc-shaped
sulfur reducing archaebacteria growing optimally at I05°C.
System. Appl. Microbiol. 4, 535-551.
[54] Pley, U., Schipka, J., Gambacorta, A. Jannasch, J.W., Fricke,
H., Rachel, R. and Stetter, K.O. (1991) Pyrodictium abyssi
sp. nov. represents a novel heterotrophic marine archaeal
hyperthermophile growing at 110°C. System. Appl. Microbiol. 14, 245-253.
[55] Zillig, W., Holz, I. Janecovic, D. Klenk, H.P., Imsel, E.,
Trent J., Wunderl, S., Forjatz, V.H., Coutinho, R. and Ferreira, T. (1990) Hyperthermus bu~licus, a hyperthermophilic
sulfur-reducing archaebacterium that ferments peptides. J.
Bacteriol. 172, 3959-3965.
[56] Zillig, W., Holz, I., Janecovic, D., Sch~ifer, W. and Reiter,
W.D. (1983)The archaebacterium Thermococcus celer represents a novel genus within the thermophilic branch of the
archaebacteria. System. Appl. Microbiol. 4, 88-94.
[57] Neuner, A., Jannasch, H.W., Belkin, S. and Stetter, K.O.
(1990) Thermococcus litoralis sp. nov. a new species of
extremely thermophilic marine archaebacteria. Arch. Microbiol. 153,205-207.
[58] Miroshnichenko, M.L., Bonch-Osmoslovskaya, E.A., Neuner, A., Kostrikina, N.A., Chernych, N.A. and Alexeyev,
V.A. (1989) Thermococcus stetteri sp. nov. a new extremely
thermophilic marine sulfur-metabolizing archaebacterium.
System. Appl. Microbiol. 12, 257-262.
[59] Kobayashi, T., Kwak, Y.S., Akiba, T., Kudo, T. and
Horikoshi, K. (1994) Thermococcus profundus sp. nov.. a
new hyperthermophilic archaeon isolated from deep-sea hydrothermal vent. System. Appl. Microbiol. 17, 232-236.
[60] Zillig, W., Holz, I., Klenk, H.P., Trent, J., Wunderl, S.,
Janekovic, D., Imsel, E. and Haas, B. (1987) Pvrococctts
woesei sp. nov., an ultra-thermophilic marine archaebacterium, represents a novel order, Thermococcales. System.
Appl. Microbiol. 9, 62-70.
[61] Stetter, K.O. (1988) Archaeglobus fulgidus gen. nov., sp.
nov.: a new taxon of extremely thermophilic archaebacteria.
System. Appl. Microbiol. 10, 172, 173.
[62] Burggraf, S., Jannasch, H.W., Nicolaus, B. and Stetter, K.O.
(1990) Archaeglobus profundus sp. nov. represents a new
species within the sulfate-reducing archaebacteria. System.
Appl. Microbiol. 13, 24-28.
[63] Stetter, K.O., Thomm, M., Winter, J., Wildgruber, G., Huber, H., Zillig, WI, Janecovic, D., Kt~nig, H. Palm, P. and
Wunderl, S. (1981) Methanothermus fervidus, sp. nov., a
novel extremely thermophilic methanogen isolated from an
Icelandic hot spring. Zentralblatt ftir Bakteriologie and Hygiene, I. Abteilung Originale C2, 166-178.
[64] Lauerer, G., Kristjansson, J.K., Langworthy, T.A., KSnig, H.
and Stetter, K.O. (1986) Methanothermus sociabilis sp. nov.,
a second species within the Methanothermaceae growing at
97°C. System. Appl. Microbiol. 8, 100-105.
[65] Huber, H., Thomm, M., Ktinig, H., Thies, G. and Stetter,
K.O. (1982) Methanococcus thermolithotrophicus, a novel
thermophilic lithotrophic methanogen. Arch. Microbiol. 132,
47-50.
[66] Jones, W.J., Leigh, J.A., Mayer, F., Woese, C.R. and Wolfe,
R.S. (1983) Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch. Microbiol. 136, 254-261.
[67] Burggraf, S., Fricke, H., Neuner, A., Kristjansson, J., Rouvier, P., Mandelco, L., Woese, C.R. and Stetter, K.O. (1990)
Methanococcus igneus sp. nov., a novel hyperthermophilic
methanogen from a shallow submarine hydrothermal system.
System. Appl. Microbiol. 13, 263-269.