A Bug's Life

[Guest guest]

A bug's life: Exceptional genomic stability yet rapid protein

evolution in a carpenter ant mutualist

WOODS HOLE, Mass., Tues., Aug. 2, 2005 – The recent surge in the

number of microbial genome sequences available to the scientific

community is allowing researchers to address interesting ecological

questions and to observe how various genomic, evolutionary, and

ecological forces interact to define an organism's role in the

environment. Today, Dr. Wernegreen's group from the Marine

Biological Laboratory presents new data that support a fascinating

model for genome evolution in bacteria that live inside insects. The

scientists show that symbiotic bacteria have undergone exceptionally

fast rates of protein evolution despite having precisely maintained

their genomic architecture over long periods of evolutionary time. In

their report, published today in the journal Genome Research, the

scientists discuss this model in the ecological context of host-

symbiont interplay.

" Symbiosis is an important driver of evolutionary novelty and

ecological diversity, " explains Wernegreen. " Microbial symbionts in

particular have been major evolutionary catalysts throughout the 4

billion years of life on earth and have largely shaped the evolution

of complex organisms. "

Symbiotic bacteria live in root nodules of leguminous plants, in

gutless marine worms, in echinoderms such as starfishes and sea

urchins, and in specialized cells of insects such as aphids and

tsetse flies. Many symbiotic relationships are obligate; neither the

bacterium nor its host can live without the other.

Wernegreen's group focused on the bacterium Blochmannia, which has

lived inside Camponotus and related ant genera for the past 30

million years or more. The bacteria may utilize the ant host for

basic metabolic functions, including the initiation of DNA

replication. In turn, the microbes may synthesize certain nutrients

that enable the ants to inhabit unique ecological niches and thrive

on nutritionally unbalanced food sources. This mutualistic

association is thought to contribute to the astounding ecological

success of Camponotus, which, with approximately 1,000 species,

represents the second largest ant genus.

By sequencing the genomes of symbiotic microbes, scientists are

currently uncovering the biological and mechanistic basis for these

mutualistic associations. One of the primary genomic characteristics

of obligate bacterial symbionts is a massive reduction in genome size

compared to their free-living counterparts – a phenomenon

called " genome streamlining. " Additional genome sequences of

bacterial symbionts are needed, however, to more fully understand the

biological basis for these associations.

Research assistants Degnan (now a doctoral student in the

Department of Ecology and Evolutionary Biology at the University of

Arizona) and Adam Lazarus worked with Wernegreen to sequence the

entire genome – all 791,654 nucleotides – of Blochmannia

pennsylvanicus, the endosymbiont that is specifically associated with

the black carpenter ant (Camponotus pennsylvanicus). In order to

trace genetic changes that occurred in the context of this ant-

bacterial mutualism, they then compared the B. pennsylvanicus genome

to the sequence from a related carpenter ant mutualist, B.

floridanus.

Although the two Blochmannia species diverged between 16 and 20

million years ago, Wernegreen's group made a striking observation:

All 635 genes shared between the two genomes were completely

conserved in terms of order and strand orientation.

This is a remarkable observation, given that bacteria are

particularly noted for their rapidly evolving genomes characterized

by extensive recombination, gene transfer, inversion, and

translocation. In comparison, the genomes of E. coli and Salmonella,

which diverged between 100-150 million years ago, have undergone

extensive changes in their genomic architecture. Interestingly, the

observations of Wernegreen regarding B. pennsylvanicus were

consistent with those previously described for the 150-200 million-

year history of Buchnera, an aphid mutualist. Taken together, these

results indicate that genome stasis may be a general feature of

insect mutualists.

Another important feature of B. pennsylvanicus tested by the

researchers was the rate of protein evolution, as measured by amino

acid changes, since the divergence of B. pennsylvanicus from their

free-living ancestors. The researchers showed that the amino acid

sequences of Blochmannia have diverged approximately 50 times more

quickly than proteins in free-living bacteria. According to the

scientists, endosymbiont proteins may be more tolerant of amino acid

changes when they first become associated with their hosts, and this

may account for the rapid rates of protein evolution observed.

In addition, protein sequences of the two Blochmannia species

exhibited different rates of evolution; divergence rates were

approximately two times faster in B. floridanus than in B.

pennsylvanicus. The authors suggested that these lineage-specific

differences may reflect life history differences of their respective

ant hosts.

When the observations of the current study are coupled with results

from previous studies, a new model for bacterial genome evolution in

the context of a host-symbiont relationship emerges. As Wernegreen

and her colleagues explain in their Genome Research article, long-

term genome stasis is a striking characteristic of insect mutualists,

and it may severely constrain the evolutionary potential of these

symbiotic microbes.

However, whether rapid rates of protein evolution are important for

the adaptation of insect mutualists remains unclear. While the

current study documents rapid changes in amino acid sequence through

evolutionary time, some studies suggest that most changes in proteins

are slightly harmful to the bacterium and by extension, to its host.

" Overall, the picture emerging is one of genome deterioration, with

the loss of many gene functions, and extreme genome stability, " says

Wernegreen. " This genomic stability may prevent the reacquisition of

those lost functions or the evolution of new ones. In addition, rapid

protein evolution seems to degrade the genes that remain. "

In the future, major areas of research will include understanding the

forces driving this mode of genome evolution, as well as the

consequences on the fitness of the bacterium and its

host. " Developments in endosymbiosis are important not only to

questions in basic research, but may have important practical

implications, " notes Wernegreen. " A very promising area of

endosymbiont research is the manipulation of these bacteria to

control host populations in the field. "