reproductive manipulation are known: feminization of genetic
males, male-killing by larval development arrest, parthenogenesis in haplodiploid Hymenoptera, and cytoplasmic incompatibility, which is a non-fertile cross between infected males with
Wolbachia and uninfected female or carrying a different strain
of Wolbachia (Werren et al. 1999). Wolbachia is thus qualified
as a parasite of the reproduction of its host. These reproductive
manipulations have resulted in biased sex ratios disadvantaging
males, thus generating more females that transmit Wolbachia
transovarially to their descendants. This explains the high prevalence of Wolbachia in natural populations of arthropods,
estimated at up to 76 % in insects (Jeyaprakash and Hoy
2000; Hilgenboecker et al. 2008). A phenotype of mutual
dependence was found in some arthropods where Wolbachia
is required for normal reproduction or development. In the
hymenopteran Asobara tabida, Wolbachia has become necessary for oogenesis in females (Dedeine et al. 2001). The elimination of Wolbachia by antibiotics generates asymbiotic
individuals completely devoid of oocytes, and ovarian tissues
showed early manifestations of apoptosis (Pannebakker et al.
2007). The bedbug, Cimex lectularius, hosts Wolbachia in a
bacteriome and the two partners seem to establish a nutritional
mutualistic symbiosis through the provisioning of vitamins
(Hosokawa et al. 2010). Remarkably, Wolbachia is also able
to protect drosophila against viral pathogens (Hedges et al.
2008), and in some cases this bacterium inhibits the transmission of pathogens by the mosquitoes (Moreira et al. 2009;
Mousson et al. 2012).
There is a unique situation where the same bacterium
induces various effects on the hosts, differing in nature and
intensity, either on their physiology or reproduction, and is
ranged in a continuum from parasitism to mutualism. These
associations thus raise many questions in evolutionary biology
(evolution of mutualism, coevolution, role in the speciation of
hosts), epidemiology (diffusion process), cell biology (cellular
targets, signaling), and molecular biology (structure, functioning, and evolution of the genome). The mechanisms underlying these interactions are unknown. Effectors secreted via the
Wolbachia T4SS (Rance `s et al. 2008) have been proposed.
Many genes encoding proteins with ankyrin domains known to
be involved in protein–protein interactions are potential
candidates present in complete genomes of Wolbachia (Wu
et al. 2004; Foster et al. 2005; Klasson et al. 2008). Transfers of
Wolbachia genes to insects and from the insect to the bacteria
have been reported following the sequencing of genomes
(Hotopp et al. 2007; Klasson et al. 2009).
11.4.4 Defense and Counteroffensive
in Microbe–Animal Interactions
Animals interacting with microbes have developed a set of
mechanisms and weapons to contain or eliminate potentially
infectious agents. These mechanisms include phagocytosis
by immune cells such as macrophages, secretion of toxic
compounds, or inhibitors such as cytokines and reactive
oxygen species. Discovered in drosophila and in many
other arthropods and vertebrates, the production of antimicrobial peptides is part of the humoral response against
microbial infection. The synthesis of antimicrobial peptides
is regulated by molecules of the nuclear factors kappa B
(NF-kappaB) family, such as DIF and Relish in Drosophila
melanogaster. Nuclear factor DIF is mainly activated in
response to fungal infection or by Gram-positive bacteria,
whereas Relish plays a role during infection by Gramnegative bacteria (Ferrandon et al. 2007).
Programmed cell death (PCD) is a manifestation of
defense commonly observed in response to infection by
microbes, either pathogenic or mutualistic (Williams 1994;
Vavre et al. 2008). In contrast, many microorganisms have
developed mechanisms to circumvent the host defenses by
detoxification, immunosuppression, or molecular mimicry
for their survival and proliferation (Silver et al. 2007).
11.4.4.1 PCD as a Means of Defense of Animals
PCD is an integral part of the development program of
higher organisms. Apoptosis* is the best known and
described PCD in insects, nematodes, and mammals
(Jacobson et al. 1997). It takes place during development
and is involved in the elimination of damaged cells and in
maintaining the homeostasis of immune cells (Vaux et al.
1994). Apoptosis involves the caspase enzymes that are
activated by many stimuli. Two apoptotic pathways are
known: the extrinsic pathway is triggered by TNFR family
receptors (Tumor Necrosis Factor Receptor) and the intrinsic
pathway that is activated by intracellular signals such as
oxidative stress and involves the disruption of mitochondria
(Fig. 11.19). From a phenotypic point of view, apoptotic
cells have their nuclear DNA fragmented.
In addition to its role in development, apoptosis is
involved in the defense against microbes and participates
in the elimination of infected cells. Its induction is initiated
after contact and perception by host cell receptors of microbial components or structures designated MAMPs (microbeassociated molecular patterns) or PAMPs (pathogenassociated molecular patterns). These components that are
specific to microorganisms are composed of lipopolysaccharide (LPS), peptidoglycan (PGN), and lipoteichoic
acids of the cell walls. Host cell receptors that are on the
front line for detecting MAMPs and PAMPS are designated
PRRs (pattern recognition receptors), the most reknown
being the Toll-like receptors or TLRs. Discovered first in
the innate antibacterial response in drosophila (Hoffmann
2003), TLR homologues were subsequently identified in
other animals including mammals (Medzhitov et al. 1997).
TLRs are also involved in the induction of apoptosis in
11 Microorganisms and Biotic Interactions
433
males, male-killing by larval development arrest, parthenogenesis in haplodiploid Hymenoptera, and cytoplasmic incompatibility, which is a non-fertile cross between infected males with
Wolbachia and uninfected female or carrying a different strain
of Wolbachia (Werren et al. 1999). Wolbachia is thus qualified
as a parasite of the reproduction of its host. These reproductive
manipulations have resulted in biased sex ratios disadvantaging
males, thus generating more females that transmit Wolbachia
transovarially to their descendants. This explains the high prevalence of Wolbachia in natural populations of arthropods,
estimated at up to 76 % in insects (Jeyaprakash and Hoy
2000; Hilgenboecker et al. 2008). A phenotype of mutual
dependence was found in some arthropods where Wolbachia
is required for normal reproduction or development. In the
hymenopteran Asobara tabida, Wolbachia has become necessary for oogenesis in females (Dedeine et al. 2001). The elimination of Wolbachia by antibiotics generates asymbiotic
individuals completely devoid of oocytes, and ovarian tissues
showed early manifestations of apoptosis (Pannebakker et al.
2007). The bedbug, Cimex lectularius, hosts Wolbachia in a
bacteriome and the two partners seem to establish a nutritional
mutualistic symbiosis through the provisioning of vitamins
(Hosokawa et al. 2010). Remarkably, Wolbachia is also able
to protect drosophila against viral pathogens (Hedges et al.
2008), and in some cases this bacterium inhibits the transmission of pathogens by the mosquitoes (Moreira et al. 2009;
Mousson et al. 2012).
There is a unique situation where the same bacterium
induces various effects on the hosts, differing in nature and
intensity, either on their physiology or reproduction, and is
ranged in a continuum from parasitism to mutualism. These
associations thus raise many questions in evolutionary biology
(evolution of mutualism, coevolution, role in the speciation of
hosts), epidemiology (diffusion process), cell biology (cellular
targets, signaling), and molecular biology (structure, functioning, and evolution of the genome). The mechanisms underlying these interactions are unknown. Effectors secreted via the
Wolbachia T4SS (Rance `s et al. 2008) have been proposed.
Many genes encoding proteins with ankyrin domains known to
be involved in protein–protein interactions are potential
candidates present in complete genomes of Wolbachia (Wu
et al. 2004; Foster et al. 2005; Klasson et al. 2008). Transfers of
Wolbachia genes to insects and from the insect to the bacteria
have been reported following the sequencing of genomes
(Hotopp et al. 2007; Klasson et al. 2009).
11.4.4 Defense and Counteroffensive
in Microbe–Animal Interactions
Animals interacting with microbes have developed a set of
mechanisms and weapons to contain or eliminate potentially
infectious agents. These mechanisms include phagocytosis
by immune cells such as macrophages, secretion of toxic
compounds, or inhibitors such as cytokines and reactive
oxygen species. Discovered in drosophila and in many
other arthropods and vertebrates, the production of antimicrobial peptides is part of the humoral response against
microbial infection. The synthesis of antimicrobial peptides
is regulated by molecules of the nuclear factors kappa B
(NF-kappaB) family, such as DIF and Relish in Drosophila
melanogaster. Nuclear factor DIF is mainly activated in
response to fungal infection or by Gram-positive bacteria,
whereas Relish plays a role during infection by Gramnegative bacteria (Ferrandon et al. 2007).
Programmed cell death (PCD) is a manifestation of
defense commonly observed in response to infection by
microbes, either pathogenic or mutualistic (Williams 1994;
Vavre et al. 2008). In contrast, many microorganisms have
developed mechanisms to circumvent the host defenses by
detoxification, immunosuppression, or molecular mimicry
for their survival and proliferation (Silver et al. 2007).
11.4.4.1 PCD as a Means of Defense of Animals
PCD is an integral part of the development program of
higher organisms. Apoptosis* is the best known and
described PCD in insects, nematodes, and mammals
(Jacobson et al. 1997). It takes place during development
and is involved in the elimination of damaged cells and in
maintaining the homeostasis of immune cells (Vaux et al.
1994). Apoptosis involves the caspase enzymes that are
activated by many stimuli. Two apoptotic pathways are
known: the extrinsic pathway is triggered by TNFR family
receptors (Tumor Necrosis Factor Receptor) and the intrinsic
pathway that is activated by intracellular signals such as
oxidative stress and involves the disruption of mitochondria
(Fig. 11.19). From a phenotypic point of view, apoptotic
cells have their nuclear DNA fragmented.
In addition to its role in development, apoptosis is
involved in the defense against microbes and participates
in the elimination of infected cells. Its induction is initiated
after contact and perception by host cell receptors of microbial components or structures designated MAMPs (microbeassociated molecular patterns) or PAMPs (pathogenassociated molecular patterns). These components that are
specific to microorganisms are composed of lipopolysaccharide (LPS), peptidoglycan (PGN), and lipoteichoic
acids of the cell walls. Host cell receptors that are on the
front line for detecting MAMPs and PAMPS are designated
PRRs (pattern recognition receptors), the most reknown
being the Toll-like receptors or TLRs. Discovered first in
the innate antibacterial response in drosophila (Hoffmann
2003), TLR homologues were subsequently identified in
other animals including mammals (Medzhitov et al. 1997).
TLRs are also involved in the induction of apoptosis in
11 Microorganisms and Biotic Interactions
433