mutualism, and syntrophy have been used for conceptually
similar phenomena. The term cooperation is sometimes used
to designate situations encompassing the other two. Mutualism is little used to describe microbe–microbe relations, but
rather is reserved for relationships between microbes and
higher organisms. The term syntrophy* would cover just
cases where microorganisms have complementary metabolisms and are in mutualistic situations, each partner
providing substrate(s) to the other(s). At one extreme of
the spectrum, there are situations of loose or non-exclusive
relationships, based on trophic exchanges thus designated
syntrophic; at the other extreme are situations of mutualism
or symbiosis involving potentially more than trophic aspects
of detoxification and entailing toxin synthesis, signaling, etc.
It has been argued that the origin of eukaryotic cells was a
syntrophy that has evolved into mutualism and finally into
an obligatory interaction (Lo ´pez-Garcı ´a and Moreira 1999).
11.2.2.1 Cometabolism
Cometabolism is a prominent case of beneficial interaction
taking place between different microorganisms. It
corresponds to cooperation, syntrophy, or even symbiosis
when metabolisms are different and complementary and
when the interaction is sustained. Microorganisms that live
in complex habitats such as soils, sediments, or digestive
tracts are typically in contact with complex trophic resources
they are unable to catabolize alone. For a single organism,
cometabolism is the transformation of a compound that
cannot serve as sole carbon and energy source (i.e., a nongrowth substrate), which is made possible by parallel degradation of a growth substrate. We also speak of cometabolism
when several microorganisms must cooperate as a consortium to synthesize all the enzymes necessary for a catabolic
pathway. This is the case of soil isolates individually unable
to metabolize polycyclic aromatic compounds, but which are
able to do so when they are grown in a consortium (Bouchez
et al. 1999). It is likely that this consortium includes strains
able to compensate for the inhibition caused by a metabolic
intermediate by degrading it or when the product of a strain
is used as a substrate by a different strain.
11.2.2.2 Mutualism
The deltaproteobacterium Syntrophus aciditrophicus can
metabolize various saturated or unsaturated fatty acids,
hexanoate and butyrate esters, or benzoate when in coculture
with microorganisms capable of metabolizing hydrogen or
formate (Mouttaki et al. 2007). Anaerobic degradation
of saturated fatty acids and aromatic acids in the absence
of a terminal electron acceptor necessitates the presence of
an organism capable of maintaining a hydrogen partial
pressure low enough so that these reactions are thermodynamically possible. We therefore find it associated with
hydrogenotrophic microorganisms such as Desulfovibrio or
the archeon Methanospirillum hungatei (cf. Chap. 3 and
Sect. 14.2.5). Mutualism is also found during methanogenesis which is a complex process described in detail in
Chaps. 3 and 14. It involves many taxa that perform various
steps in the complex pathway that transforms organic
compounds into acetate and eventually into methane (cf.
Sects. 3.3 and 14.2.5).
Sometimes the metabolic basis of the association is
unknown, as in the case of the two archaea Nanoarchaeum
equitans (Nanoarchaeota; cf. Chap. 6) and Ignicoccus
hospitalis (Crenarchaeota) present in hydrothermal environments, which are in close interaction in a relationship
described as symbiosis or parasitism (Jahn et al. 2008).
These two organisms are closely nested into one another and
cannot be cultured separately. Another interesting case
concerns Symbiobacterium thermophilum (Firmicute)
(Watsuji et al. 2006), which cannot be cultivated in the absence
of a Bacillus sp. Both thermophilic bacteria are found in
composts. Bacillus sp. provides S. thermophilum with CO 2
from its respiration, which allows S. thermophilum to compensate for the absence of a carbonic anhydrase, an enzyme that
allows different processes such as photosynthesis, respiration,
pH homeostasis, and ion transport. It also catabolizes indolic
compounds, which are self-inhibitors to S. thermophilum. The
advantage for the Bacillus sp. is not clear; it may simply be a
situation of commensalism or catabolism of recalcitrant
compounds found in the compost.
Mutualism is not restricted to catabolic functions. Sometimes, diseases of plants and animals are caused by consortia
or teams consisting of very different partners. This is the case
of seedling blight of rice, caused by the fungus Rhizopus
microsporus, which contains in its cytoplasm endosymbiotic
Burkholderia bacteria necessary for production of the virulence factor rhizotoxin and plant disease (Partida-Martinez
and Hertweck 2005). The presence of Burkholderia within
fungal tissues has been reported in many fungi.
Biofilms (cf. Sect. 9.7.3) found in soils, sediments, higher
organisms, and man-made environments are complex
assemblies that can include many taxa, some more active
than others for the synthesis of exopolysaccharides. These
polymers, which trap heavy metals or antibiotics, allow the
development of a three-dimensional structure and protect all
cells present, those synthesizing the polymers as well as the
others. Microbial mats (cf. Sect. 9.7.3) include many microbial
taxa with complementary physiological properties such as
sulfate reduction and sulfate oxidation, photosynthesis, and
heterotrophy. Despite the synthesis in these mats of
compounds with antibiotic activity (Socha et al. 2007), the
taxa present complement and protect each other during the
development of microbial mats (Fourcans et al. 2006) and are
therefore in situations of mutualism.
11 Microorganisms and Biotic Interactions
403
similar phenomena. The term cooperation is sometimes used
to designate situations encompassing the other two. Mutualism is little used to describe microbe–microbe relations, but
rather is reserved for relationships between microbes and
higher organisms. The term syntrophy* would cover just
cases where microorganisms have complementary metabolisms and are in mutualistic situations, each partner
providing substrate(s) to the other(s). At one extreme of
the spectrum, there are situations of loose or non-exclusive
relationships, based on trophic exchanges thus designated
syntrophic; at the other extreme are situations of mutualism
or symbiosis involving potentially more than trophic aspects
of detoxification and entailing toxin synthesis, signaling, etc.
It has been argued that the origin of eukaryotic cells was a
syntrophy that has evolved into mutualism and finally into
an obligatory interaction (Lo ´pez-Garcı ´a and Moreira 1999).
11.2.2.1 Cometabolism
Cometabolism is a prominent case of beneficial interaction
taking place between different microorganisms. It
corresponds to cooperation, syntrophy, or even symbiosis
when metabolisms are different and complementary and
when the interaction is sustained. Microorganisms that live
in complex habitats such as soils, sediments, or digestive
tracts are typically in contact with complex trophic resources
they are unable to catabolize alone. For a single organism,
cometabolism is the transformation of a compound that
cannot serve as sole carbon and energy source (i.e., a nongrowth substrate), which is made possible by parallel degradation of a growth substrate. We also speak of cometabolism
when several microorganisms must cooperate as a consortium to synthesize all the enzymes necessary for a catabolic
pathway. This is the case of soil isolates individually unable
to metabolize polycyclic aromatic compounds, but which are
able to do so when they are grown in a consortium (Bouchez
et al. 1999). It is likely that this consortium includes strains
able to compensate for the inhibition caused by a metabolic
intermediate by degrading it or when the product of a strain
is used as a substrate by a different strain.
11.2.2.2 Mutualism
The deltaproteobacterium Syntrophus aciditrophicus can
metabolize various saturated or unsaturated fatty acids,
hexanoate and butyrate esters, or benzoate when in coculture
with microorganisms capable of metabolizing hydrogen or
formate (Mouttaki et al. 2007). Anaerobic degradation
of saturated fatty acids and aromatic acids in the absence
of a terminal electron acceptor necessitates the presence of
an organism capable of maintaining a hydrogen partial
pressure low enough so that these reactions are thermodynamically possible. We therefore find it associated with
hydrogenotrophic microorganisms such as Desulfovibrio or
the archeon Methanospirillum hungatei (cf. Chap. 3 and
Sect. 14.2.5). Mutualism is also found during methanogenesis which is a complex process described in detail in
Chaps. 3 and 14. It involves many taxa that perform various
steps in the complex pathway that transforms organic
compounds into acetate and eventually into methane (cf.
Sects. 3.3 and 14.2.5).
Sometimes the metabolic basis of the association is
unknown, as in the case of the two archaea Nanoarchaeum
equitans (Nanoarchaeota; cf. Chap. 6) and Ignicoccus
hospitalis (Crenarchaeota) present in hydrothermal environments, which are in close interaction in a relationship
described as symbiosis or parasitism (Jahn et al. 2008).
These two organisms are closely nested into one another and
cannot be cultured separately. Another interesting case
concerns Symbiobacterium thermophilum (Firmicute)
(Watsuji et al. 2006), which cannot be cultivated in the absence
of a Bacillus sp. Both thermophilic bacteria are found in
composts. Bacillus sp. provides S. thermophilum with CO 2
from its respiration, which allows S. thermophilum to compensate for the absence of a carbonic anhydrase, an enzyme that
allows different processes such as photosynthesis, respiration,
pH homeostasis, and ion transport. It also catabolizes indolic
compounds, which are self-inhibitors to S. thermophilum. The
advantage for the Bacillus sp. is not clear; it may simply be a
situation of commensalism or catabolism of recalcitrant
compounds found in the compost.
Mutualism is not restricted to catabolic functions. Sometimes, diseases of plants and animals are caused by consortia
or teams consisting of very different partners. This is the case
of seedling blight of rice, caused by the fungus Rhizopus
microsporus, which contains in its cytoplasm endosymbiotic
Burkholderia bacteria necessary for production of the virulence factor rhizotoxin and plant disease (Partida-Martinez
and Hertweck 2005). The presence of Burkholderia within
fungal tissues has been reported in many fungi.
Biofilms (cf. Sect. 9.7.3) found in soils, sediments, higher
organisms, and man-made environments are complex
assemblies that can include many taxa, some more active
than others for the synthesis of exopolysaccharides. These
polymers, which trap heavy metals or antibiotics, allow the
development of a three-dimensional structure and protect all
cells present, those synthesizing the polymers as well as the
others. Microbial mats (cf. Sect. 9.7.3) include many microbial
taxa with complementary physiological properties such as
sulfate reduction and sulfate oxidation, photosynthesis, and
heterotrophy. Despite the synthesis in these mats of
compounds with antibiotic activity (Socha et al. 2007), the
taxa present complement and protect each other during the
development of microbial mats (Fourcans et al. 2006) and are
therefore in situations of mutualism.
11 Microorganisms and Biotic Interactions
403