hydrogen as electron donors and nitrate as electron acceptor.
It also grows heterotrophically on acetate under aerobic and
denitrifying conditions. This is a clear demonstration of a
remarkable metabolic versatility possibly existing in the
group of haloalkaliphilic Gammaproteobacteria which was
not reported so far.
Screening of many alkaline lakes with high salinity in different parts of the world indicated that haloalkaliphilic archaea
belonging to the family Halobacteriaceae, also known under
the generic name of “halobacteria” or “haloarchaea,” were
always present in such environments. These microorganisms
are the most halophiles that we know. They are part of the
dominant microflora when salinity conditions reach saturation.
They are responsible for the red color of the water due to their
carotenoid content. The soda lakes are inhabited by members of
the genera Natronobacterium, Natronococcus, Natronomonas,
Natrialba, Natrorubrum, and Halorubrum (Wiegel 2011).
10.7.3.3 Alkaliphilic Anaerobic Microflora
Compared to aerobic environments, haloalkaline anaerobic
environments have been poorly studied. A biological process that predominates in soda lakes is sulfate reduction.
This process is responsible in not just the final stage of
degradation of organic matter but also, in part, the conditions
that generate alkalinity as a result of the conversion of
sulfate to sulfide. The first alkaliphilic sulfate-reducing bacterium Desulfonatronovibrio hydrogenovorans, a member of
the Deltaproteobacteria, was isolated from the soda lake
Magadi in Kenya. This species was also found in the soda
lakes of the region of Tuva in Central Asia, which prompted
some authors to suggest that this species might play a universal role as final hydrogen acceptor in alkaliphilic anaerobic communities producing sulfide. Another sulfate-reducer
member of the Deltaproteobacteria, Desulfonatronum
lacustre, was isolated from an oligotrophic alkaline lake,
the lake Khadyn (Tuva). Both genera comprise mesophilic
nonsporulated Gram-negative species, which require the
presence of carbonate, and are unable to grow at pH values
below 8. A spore-forming alkaliphilic and moderately thermophilic sulfate reducer, Desulfotomaculum alkaliphilum,
was isolated from pig slurry at neutral pH, indicating that
the adaptation of microorganisms to alkaline environments
does not result from important genetic changes.
There is no doubt that methanogenesis occurs in soda
lakes. To date, the methanoarchaea isolated from soda
lakes are predominantly methylotrophic microorganisms
using methylated compounds such as methanol or
methylamines. These compounds are abundant in soda
lakes. They probably originated from the anaerobic degradation of cyanobacterial mats and/or from compatible
solutes (e.g., betaine and ectoine) transported or synthesized
by alkaliphilic organotrophs. Methylotrophic methanoarchaea
isolated from several soda lakes with salt concentrations close
to saturation belong to the genera Methanosalsus and
Methanohalophilus, family Methanosarcinaceae, phylum
Euryarchaeota. Hydrogenotrophic methanogens within
genus Methanobacterium were also identified in several
soda lakes. However, these microorganisms appear to be
alkalitolerant rather than true alkaliphiles. Generally, studies
on alkaliphilic methanogens reveal that methanogenesis from
H 2 /CO 2 increases when salinity decreases, while under high
salinity conditions, methanogenesis from methylamines
predominates.
Acetogenesis (Natroniella acetigena) and nitrate reduction
(Halomonas campisalis, Thioalkalivibrio nitratireducens) are
metabolic activities already detected in alkaline environments.
Natroniella acetigena is a haloalkaliphilic bacterium, which
belongs to Halobacteroidaceae (order Halanaerobiales).
Halonatronum saccharophilum, a chemoorganotrophic moderately haloalkaliphilic member of this order, was isolated
from sediments of the lake Magadi, and more recently, the
first alkaliphilic anaerobic hydrogenotrophic homoacetogenic
bacterium (Fuchsiella alkaliacetigena) was isolated from
sediments of the soda-depositing soda lake Tanatar III
(Altay, Russia).
Microorganisms fermenting aminoacids were isolated in
soda lakes. Both species Natronincola histidinovorans and
Tindallia magadiensis were also isolated from lake Magadi.
They are closely phylogenetically related to the group XI of
the Clostridium taxon.
10.7.4 Homeostasis of the pH
Alkaliphilic bacteria have to face a bioenergetical problem
which arised from the necessity of maintaining a cytoplasmic pH that is much lower than optimal external pH for
growth. These bacteria have developed during the course
of evolution adaptation mechanisms to prevent alkalinization of their cytoplasm. Regulatory mechanisms of ion transport exist in the cell membrane. In normal conditions, these
mechanisms maintain the cytoplasmic pH in a narrow range
around neutrality, even when the extracellular pH varies
significantly. They are known under the term “pH homeostasis” (Krulwich et al. 2011).
Alkaliphilic microorganisms, which grow abundantly at a
pH higher than 9, require the presence of Na
+ ions in the
surrounding environment for the effective transport of
solutes across the cytoplasmic membrane. Studies on
alkaliphilic Bacillus showed that a Na
+ gradient provided
the energy necessary to transport and motility by the creation
of a proton-motive force engendering ATP synthesis.
According to the chemiosmotic hypothesis, proton-motive
force in the cell is generated by the electron transport chain
or by the excretion of protons originated from ATP metabolism by the ATP synthase. The protons are then reintroduced
390
J.-L. Cayol et al.
It also grows heterotrophically on acetate under aerobic and
denitrifying conditions. This is a clear demonstration of a
remarkable metabolic versatility possibly existing in the
group of haloalkaliphilic Gammaproteobacteria which was
not reported so far.
Screening of many alkaline lakes with high salinity in different parts of the world indicated that haloalkaliphilic archaea
belonging to the family Halobacteriaceae, also known under
the generic name of “halobacteria” or “haloarchaea,” were
always present in such environments. These microorganisms
are the most halophiles that we know. They are part of the
dominant microflora when salinity conditions reach saturation.
They are responsible for the red color of the water due to their
carotenoid content. The soda lakes are inhabited by members of
the genera Natronobacterium, Natronococcus, Natronomonas,
Natrialba, Natrorubrum, and Halorubrum (Wiegel 2011).
10.7.3.3 Alkaliphilic Anaerobic Microflora
Compared to aerobic environments, haloalkaline anaerobic
environments have been poorly studied. A biological process that predominates in soda lakes is sulfate reduction.
This process is responsible in not just the final stage of
degradation of organic matter but also, in part, the conditions
that generate alkalinity as a result of the conversion of
sulfate to sulfide. The first alkaliphilic sulfate-reducing bacterium Desulfonatronovibrio hydrogenovorans, a member of
the Deltaproteobacteria, was isolated from the soda lake
Magadi in Kenya. This species was also found in the soda
lakes of the region of Tuva in Central Asia, which prompted
some authors to suggest that this species might play a universal role as final hydrogen acceptor in alkaliphilic anaerobic communities producing sulfide. Another sulfate-reducer
member of the Deltaproteobacteria, Desulfonatronum
lacustre, was isolated from an oligotrophic alkaline lake,
the lake Khadyn (Tuva). Both genera comprise mesophilic
nonsporulated Gram-negative species, which require the
presence of carbonate, and are unable to grow at pH values
below 8. A spore-forming alkaliphilic and moderately thermophilic sulfate reducer, Desulfotomaculum alkaliphilum,
was isolated from pig slurry at neutral pH, indicating that
the adaptation of microorganisms to alkaline environments
does not result from important genetic changes.
There is no doubt that methanogenesis occurs in soda
lakes. To date, the methanoarchaea isolated from soda
lakes are predominantly methylotrophic microorganisms
using methylated compounds such as methanol or
methylamines. These compounds are abundant in soda
lakes. They probably originated from the anaerobic degradation of cyanobacterial mats and/or from compatible
solutes (e.g., betaine and ectoine) transported or synthesized
by alkaliphilic organotrophs. Methylotrophic methanoarchaea
isolated from several soda lakes with salt concentrations close
to saturation belong to the genera Methanosalsus and
Methanohalophilus, family Methanosarcinaceae, phylum
Euryarchaeota. Hydrogenotrophic methanogens within
genus Methanobacterium were also identified in several
soda lakes. However, these microorganisms appear to be
alkalitolerant rather than true alkaliphiles. Generally, studies
on alkaliphilic methanogens reveal that methanogenesis from
H 2 /CO 2 increases when salinity decreases, while under high
salinity conditions, methanogenesis from methylamines
predominates.
Acetogenesis (Natroniella acetigena) and nitrate reduction
(Halomonas campisalis, Thioalkalivibrio nitratireducens) are
metabolic activities already detected in alkaline environments.
Natroniella acetigena is a haloalkaliphilic bacterium, which
belongs to Halobacteroidaceae (order Halanaerobiales).
Halonatronum saccharophilum, a chemoorganotrophic moderately haloalkaliphilic member of this order, was isolated
from sediments of the lake Magadi, and more recently, the
first alkaliphilic anaerobic hydrogenotrophic homoacetogenic
bacterium (Fuchsiella alkaliacetigena) was isolated from
sediments of the soda-depositing soda lake Tanatar III
(Altay, Russia).
Microorganisms fermenting aminoacids were isolated in
soda lakes. Both species Natronincola histidinovorans and
Tindallia magadiensis were also isolated from lake Magadi.
They are closely phylogenetically related to the group XI of
the Clostridium taxon.
10.7.4 Homeostasis of the pH
Alkaliphilic bacteria have to face a bioenergetical problem
which arised from the necessity of maintaining a cytoplasmic pH that is much lower than optimal external pH for
growth. These bacteria have developed during the course
of evolution adaptation mechanisms to prevent alkalinization of their cytoplasm. Regulatory mechanisms of ion transport exist in the cell membrane. In normal conditions, these
mechanisms maintain the cytoplasmic pH in a narrow range
around neutrality, even when the extracellular pH varies
significantly. They are known under the term “pH homeostasis” (Krulwich et al. 2011).
Alkaliphilic microorganisms, which grow abundantly at a
pH higher than 9, require the presence of Na
+ ions in the
surrounding environment for the effective transport of
solutes across the cytoplasmic membrane. Studies on
alkaliphilic Bacillus showed that a Na
+ gradient provided
the energy necessary to transport and motility by the creation
of a proton-motive force engendering ATP synthesis.
According to the chemiosmotic hypothesis, proton-motive
force in the cell is generated by the electron transport chain
or by the excretion of protons originated from ATP metabolism by the ATP synthase. The protons are then reintroduced
390
J.-L. Cayol et al.