sequences of oomycete species (filamentous parasites
belonging to the phylum Heterokonta) has shown the presence of 11 genes acquired by HGT from filamentous fungi
(Richards et al. 2006). Most of these genes have functions
involved in osmotrophy, which suggests that this nutritional
character may have evolved secondarily in oomycetes by
convergence with fungi thanks to the transfer of those genes.
These examples show the importance of HGT in the adaptation of eukaryotes to new ecological niches.
12.5 Conclusion
Horizontal gene transfer and the mechanisms associated
have been discovered during the first half of the twentieth
century. Despite intensive studies, the detailed molecular
mechanisms have not been completely understood. This is
nevertheless a fundamental question in biology as HGT
plays a major role in the adaptation of microorganisms to
their environment. However, microbiologists have considered for a long time that this phenomenon was restricted to
genes involved in the rapid adaptation of prokaryotes to
sudden changes in their ecosystems. The arrival of the
genome era has revealed that the quantitative and qualitative
significance of HGT had been underestimated. In fact, HGTs
get rid of the geographical barriers allowing the exchange of
genetic material among individuals living in different
ecosystems. Similarly, through the acquisition of genes
from donors belonging to different species, HGT has compelled to reexamine the barriers between species, a central
concept in biology. It has also been demonstrated that HGT
affects all living beings, including eukaryotes.
Today, most evolutionists consider that HGT has
contributed (and still contributes) to build up the prokaryotic
genomes. The most fervent advocates propose that HGT is
so dominant that concepts as notion of species or of evolution have to be completely revised. However, there is a
debate on this topic in the scientific community that is still
alive and far from settled, so that a cautious approach to
these questions remains necessary. For example, despite the
increasing availability of genome data and the improvement
of detection methods, the accurate quantification of HGT
remains very difficult to achieve. There are multiple methodological problems, and, up to now, any approach has not
been able to provide a satisfying solution. In addition, even if
HGT is frequent, it is important to remind that genes also
experience a vertical evolution. For example, the E. coli
strains K12 and O157:H7 have about 200 different genome
fragments (~30 % of their genomes), which most likely
correspond to ~200 events of insertion or deletion linked to
HGT. Knowing that the two strains diverged ~10 million
years ago, this corresponds to an HGT event every 2 Â 10
7
/
200 ¼ 10
5 years. Assuming 100 generations per year for this
bacterial species, the number of generations that have
existed since the divergence of the two strains is of
10
7
 100 ¼ 10
9 . Thus, vertical inheritance is much more
frequent than horizontal transfer. This implies that even if
HGT is common at the scale of complete genomes, it has to
be cautiously considered by taking into account that it has
occurred over very long time spans.
The development, commercialization, and massive utilization of a large number of new antibiotics, fungicides, and
biotechnological molecules have induced a strong selection
pressure on microorganisms. These can use HGT as a way to
adapt as they did before the arrival of these human-induced
stresses. Large-scale analyses of genomes and metagenomes
will allow in forthcoming years acquiring a better knowledge on the processes and the prevalence of HGT in the
environment.
References
Adams KL, Qiu YL, Stoutemyer M, Palmer JD (2002) Punctuated
evolution of mitochondrial gene content: high and variable rates
of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci U S A 99:9905–9912
Andersson JO et al (2007) A genomic survey of the fish parasite
Spironucleus salmonicida indicates genomic plasticity among
diplomonads and significant lateral gene transfer in eukaryote
genome evolution. BMC Genomics 8:51
Aravind L, Tatusov RL, Wolf YI, Walker DR, Koonin EV (1998)
Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet 14:442–444
Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ (2003)
Lateral gene transfer and the evolution of plastid-targeted proteins
in the secondary plastid-containing alga Bigelowiella natans. Proc
Natl Acad Sci U S A 100:7678–7683
Avery OT, MacLeod CM, McCarty M (1944) Studies on the chemical
nature of the substance inducing transformation of pneumococcal
types. Induction of transformation by a deoxyribonucleic acid fraction isolated from Pneumococcus type III. J Exp Med 79:137–158
Bapteste E et al (2009) Prokaryotic evolution and the tree of life are two
different things. Biol Direct 4:34
Barlow M (2009) What antimicrobial resistance has taught us about
horizontal gene transfer. Methods Mol Biol 532:397–411
Berriman M et al (2005) The genome of the African trypanosome
Trypanosoma brucei. Science 309:416–422
Bhavnani SM, Hammel JP, Jones RN, Ambrose PG (2005) Relationship between increased levofloxacin use and decreased susceptibility of Streptococcus pneumoniae in the United States. Diagn
Microbiol Infect Dis 51:31–37
Brochier-Armanet C, Forterre P (2007) Widespread distribution of
archaeal reverse gyrase in thermophilic bacteria suggests a complex
history of vertical inheritance and lateral gene transfers. Archaea
2:83–93
Brochier-Armanet C, Deschamps P, Lo ´pez-Garcı ´a P, Zivanovic Y,
Rodrı ´guez-Valera F, Moreira D (2011) Complete-fosmid and
fosmid-end sequences reveal frequent horizontal gene transfers in
marine uncultured planktonic archaea. ISME J 5:1291–1302
Burge C, Campbell AM, Karlin S (1992) Over- and underrepresentation of short oligonucleotides in DNA sequences. Proc
Natl Acad Sci U S A 89:1358–1362
12 Horizontal Gene Transfer in Microbial Ecosystems
479
belonging to the phylum Heterokonta) has shown the presence of 11 genes acquired by HGT from filamentous fungi
(Richards et al. 2006). Most of these genes have functions
involved in osmotrophy, which suggests that this nutritional
character may have evolved secondarily in oomycetes by
convergence with fungi thanks to the transfer of those genes.
These examples show the importance of HGT in the adaptation of eukaryotes to new ecological niches.
12.5 Conclusion
Horizontal gene transfer and the mechanisms associated
have been discovered during the first half of the twentieth
century. Despite intensive studies, the detailed molecular
mechanisms have not been completely understood. This is
nevertheless a fundamental question in biology as HGT
plays a major role in the adaptation of microorganisms to
their environment. However, microbiologists have considered for a long time that this phenomenon was restricted to
genes involved in the rapid adaptation of prokaryotes to
sudden changes in their ecosystems. The arrival of the
genome era has revealed that the quantitative and qualitative
significance of HGT had been underestimated. In fact, HGTs
get rid of the geographical barriers allowing the exchange of
genetic material among individuals living in different
ecosystems. Similarly, through the acquisition of genes
from donors belonging to different species, HGT has compelled to reexamine the barriers between species, a central
concept in biology. It has also been demonstrated that HGT
affects all living beings, including eukaryotes.
Today, most evolutionists consider that HGT has
contributed (and still contributes) to build up the prokaryotic
genomes. The most fervent advocates propose that HGT is
so dominant that concepts as notion of species or of evolution have to be completely revised. However, there is a
debate on this topic in the scientific community that is still
alive and far from settled, so that a cautious approach to
these questions remains necessary. For example, despite the
increasing availability of genome data and the improvement
of detection methods, the accurate quantification of HGT
remains very difficult to achieve. There are multiple methodological problems, and, up to now, any approach has not
been able to provide a satisfying solution. In addition, even if
HGT is frequent, it is important to remind that genes also
experience a vertical evolution. For example, the E. coli
strains K12 and O157:H7 have about 200 different genome
fragments (~30 % of their genomes), which most likely
correspond to ~200 events of insertion or deletion linked to
HGT. Knowing that the two strains diverged ~10 million
years ago, this corresponds to an HGT event every 2 Â 10
7
/
200 ¼ 10
5 years. Assuming 100 generations per year for this
bacterial species, the number of generations that have
existed since the divergence of the two strains is of
10
7
 100 ¼ 10
9 . Thus, vertical inheritance is much more
frequent than horizontal transfer. This implies that even if
HGT is common at the scale of complete genomes, it has to
be cautiously considered by taking into account that it has
occurred over very long time spans.
The development, commercialization, and massive utilization of a large number of new antibiotics, fungicides, and
biotechnological molecules have induced a strong selection
pressure on microorganisms. These can use HGT as a way to
adapt as they did before the arrival of these human-induced
stresses. Large-scale analyses of genomes and metagenomes
will allow in forthcoming years acquiring a better knowledge on the processes and the prevalence of HGT in the
environment.
References
Adams KL, Qiu YL, Stoutemyer M, Palmer JD (2002) Punctuated
evolution of mitochondrial gene content: high and variable rates
of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci U S A 99:9905–9912
Andersson JO et al (2007) A genomic survey of the fish parasite
Spironucleus salmonicida indicates genomic plasticity among
diplomonads and significant lateral gene transfer in eukaryote
genome evolution. BMC Genomics 8:51
Aravind L, Tatusov RL, Wolf YI, Walker DR, Koonin EV (1998)
Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet 14:442–444
Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ (2003)
Lateral gene transfer and the evolution of plastid-targeted proteins
in the secondary plastid-containing alga Bigelowiella natans. Proc
Natl Acad Sci U S A 100:7678–7683
Avery OT, MacLeod CM, McCarty M (1944) Studies on the chemical
nature of the substance inducing transformation of pneumococcal
types. Induction of transformation by a deoxyribonucleic acid fraction isolated from Pneumococcus type III. J Exp Med 79:137–158
Bapteste E et al (2009) Prokaryotic evolution and the tree of life are two
different things. Biol Direct 4:34
Barlow M (2009) What antimicrobial resistance has taught us about
horizontal gene transfer. Methods Mol Biol 532:397–411
Berriman M et al (2005) The genome of the African trypanosome
Trypanosoma brucei. Science 309:416–422
Bhavnani SM, Hammel JP, Jones RN, Ambrose PG (2005) Relationship between increased levofloxacin use and decreased susceptibility of Streptococcus pneumoniae in the United States. Diagn
Microbiol Infect Dis 51:31–37
Brochier-Armanet C, Forterre P (2007) Widespread distribution of
archaeal reverse gyrase in thermophilic bacteria suggests a complex
history of vertical inheritance and lateral gene transfers. Archaea
2:83–93
Brochier-Armanet C, Deschamps P, Lo ´pez-Garcı ´a P, Zivanovic Y,
Rodrı ´guez-Valera F, Moreira D (2011) Complete-fosmid and
fosmid-end sequences reveal frequent horizontal gene transfers in
marine uncultured planktonic archaea. ISME J 5:1291–1302
Burge C, Campbell AM, Karlin S (1992) Over- and underrepresentation of short oligonucleotides in DNA sequences. Proc
Natl Acad Sci U S A 89:1358–1362
12 Horizontal Gene Transfer in Microbial Ecosystems
479