Biology Reference
In-Depth Information
MECHANISMS OF PROKARYOTE-EUKARYOTE
HORIZONTAL GENE TRANSFER: “FOOD HYPOTHESIS”
AND “ENDOSYMBIONT HYPOTHESIS”
Mechanisms of horizontal gene transfer between prokaryotes, such as transformation, trans-
duction, and conjugation, are relatively well understood (Ochman et al., 2000; Bushman, 2002).
In contrast, mechanisms underlying prokaryoteÏeukaryote gene transfer are unknown, although
several hypothetical models have been considered. One model is the Ñfood hypothesis,Ò which
applies to prokaryotic genes identiÝed in phagocytic unicellular eukaryotes like
Trichomonas
and
Entamoeba
(Kning et al., 2000; Field et al., 2000; Andersson et al., 2001). Unicellular
eukaryotes often live close to prokaryotes and frequently use them as food, which means that
they are constantly exposed to prokaryotic DNA (Doolittle, 1998; Berg and Kurland, 2000).
However, this model does not appear applicable to multicellular eukaryotes like animals
because foreign prokaryotes are not easily accessible to the germ line cells due to germ-soma
separation and absence of active phagocytosis. An alternative model, the Ñendosymbiont
hypothesis,Ò which rests on the assumption of permanent contact between eukaryotic host cells
and inhabiting microbial associates, may apply to these cases. In fact, mitochondria and
chloroplasts have experienced gene transfer to the nucleus accompanied by drastic reduction
in their genome size at early stages of their endosymbiotic evolution (Martin et al., 1998; Gray
et al., 1999). In plants and animals, transfer of mitochondrial genes to the nuclear genome has
been shown to be a currently ongoing process (Palmer et al., 2000; Bensasson et al., 2001). It
appears meaningful that obligate endosymbiotic bacteria tend to exhibit a remarkably reduced
genome size in comparison with their free-living relatives (Andersson and Kurland, 1998;
Andersson et al., 1998; Shigenobu et al., 2000; Ochman and Moran, 2001). However, no case
of horizontal gene transfer from prokaryotic endosymbiont to eukaryotic host has been
described to date.
HORIZONTAL GENOME TRANSFER FROM
WOLBACHIA
ENDOSYMBIONT TO X CHROMOSOME OF
C. CHINENSIS
In this study, we have provided unequivocal evidence of horizontal gene transfer from an
endosymbiotic bacterium of the genus
Wolbachia
to a bruchid beetle. This Ýnding is the Ýrst
authentic case of horizontal gene transfer between prokaryotic endosymbiont and multicellular
eukaryotic host. The horizontal transfer event we discovered is unprecedented in that (1) the
transfer must be a recent event, (2) the donor bacterium is unequivocally identiÝed as
Wolbachia
,
(3) a large fragment of bacterial genome was transferred, (4) the structure of the transferred
bacterial genome is highly preserved, and (5) the location of the transferred genome fragment
has been identiÝed as the X chromosome.
INACTIVATED
WOLBACHIA
GENES ON HOST CHROMOSOME
Of the 12 ORFs identiÝed on the
Wolbachia
genome fragment (excluding the non-LTR retrotrans-
poson region), more than half (7 ORFs) contained stop codons or frame-shift substitutions, although
these ORFs in the wMel genome were structurally intact (
Figure 18.12)
.
Preliminary RT-PCR
analyses showed that
wsp
and
ftsZ
were not transcribed in the strain jC
Aus
(data not shown). These
results indicate that most of the
Wolbachia
genes became pseudogenes upon or after the horizontal
transfer and are no longer functional. However, it is unknown whether all the transferred
Wolbachia
genes are inactivated or whether some of them survive on the host chromosome. It will be necessary
to clone the whole
Wolbachia
genome fragment, to determine its structure, and to examine the
expression of all ORFs on the fragment.
