Photo: A variant of Serpula lacrymans causes dry rot. (Dave Brown via Flickr/Creative Commons Attribution 2.0) |
Feared
by realtors and homeowners alike, dry rot due to the fungus Serpula
lacrymans causes millions of dollars worth of damage to homes and
buildings around the world. This brown rot fungus’ capacity to break
down the cellulose in wood led to its selection for sequencing by the
U.S. Department of Energy (DOE) Joint Genome Institute (JGI) in 2007,
with the goal of identifying the enzymes involved in the degradation
process and using the information to improve cellulosic biofuels
production.
As
reported online in Science Express, an international team of
scientists including DOE JGI researchers compared the genome of Serpula
lacrymans, the second brown rot fungus to have its genome sequenced,
against 10 other published fungal genomes. The DOE JGI sequenced seven
of these genomes among them Postia placenta, the first brown rot fungus
sequenced. The analysis not only allowed researchers to understand the
chemical reactions involved in the mechanism by which Serpula breaks
down cellulose, it also sheds light on the role of brown rot fungi in
the development of the largest terrestrial ecosystem—the subarctic
cool climate boreal forest—and therefore the fungi’s role in the
global carbon cycle.
“It’s
one of those fungi that everybody knows. It has such an aggressive form
of cellulose breakdown,” says study first author Dan Eastwood of
Swansea University.
He
pointed out that the ability of wood-decaying fungi in general to break
down lignocellulose is linked to the co-evolution of boreal forests and
fungi.
“It
is also important to realize the role of these fungi in the natural
environment,” he says. “For example, if you go back far enough in time
to the period when trees were developing, there was no way to break
lignocellulose down, which led to the coal seams we tap today. When the
fungi figured out how to break down lignocellulose, the coevolution of
the fungi and trees kick-started the carbon cycle again. The ancestor of
all wood decay fungi we have today was a white rot and it was fungi
derived from this ancestor which kick started the carbon cycle and
lignocellulose decomposition. The brown rots evolved later from a white
rot ancestry and, because they circumvent the lignin and go straight for
the hemicellulose and cellulose, they are considered more efficient and
is probably why they have been able to dominate boreal forests in more
recent times.”
The
analyses of the 48.2-million nucleotide genome of S. lacrymans not only
allowed the team to compare the gene families involved in the
mechanisms by which brown rot break down cellulose and white rot fungi
break down both cellulose and lignin, but also how these processes
differ within each category. For example, Eastwood noted that the
chemistry Serpula uses is slightly different from the chemistry that
goes on in Postia, though in a larger sense between white rot and brown
rot, “what we describe here is a refinement of the genes, what genes are
absolutely necessary to break down cellulose,” he says. “Part of that
is the machinery to break down wood became simpler since brown rot fungi
are not breaking down lignin.”
Study
senior author Sarah Watkinson of the University of Oxford emphasized
the role of brown rot fungi in the global carbon cycle, noting that a
third of the carbon sequestered in the soil of boreal forests are
composed of the wood residues after the fungi break down the cellulose.
“When
it grows in forests, it decays the wood and leaves behind the lignin,”
she says. “We’re very interested in what puts carbon into the soil as
the residues of brown rot fungi contribute up to 30% of carbon in
conifer forest soils, and conifer forests are a very large biome in the
world and one of the largest carbon sinks on land. The activity of
brown rot is very significant in global carbon cycling and I think that
hasn’t really been appreciated before.”
Eastwood
added that the work impacts so many different fields, deciding what to
do next is “like being a child in a sweet shop: where do we start?” One
application that Jonathan Schilling, a professor at the University of
Minnesota who was not involved in the project, sees for the Serpula
genome is that itcan teach bioenergy researchers about improving the
process by which plant biomass is converted for biofuel production.
Photo:Tree in a Wyoming old growth forest decomposing due to brown rot. (Sarah Watkinson, University of Oxford) |
“What
we have right now with current bioconversion processes often resembles a
white rot approach,” he says, “attacking lignin to get at carbohydrates
and then converting them to fuels, chemicals, or paper. The brown rot
fungi have somehow circumvented that step to more efficiently get at the
cellulose instead of blasting lignin, and it has evolved multiple times
in different white rot lineages. This suggests an upgrade in efficiency
and we should pay attention.”
He
also says that having a second brown rot genome reference data set,
particularly one from such a well-studied fungus that has retained some
familiar cellulolytic mechanisms for white rot yet causes a classic
brown rot, adds on to the body of knowledge researchers have for the six
different lineages of brown rot fungi and their adaptive advantages to
white rot fungi.
DOE
JGI Fungal Genomics head Igor Grigoriev, a coauthor on the Science
paper, noted that having the genome of Serpula means that there are now
two white rot and two brown rot genomes available, and a dozen more are
in queue. He added there are two variants of Serpula, the one that
causes dry rot and one found in coniferous forests, and the DOE JGI has
sequenced both. In fact, the Institute’s sequencing efforts account for
40% of all fungal genomes deposited in the public databases.
“This
is a step forward into learning more about the processes involved in
cellulose degradation,” he says. Beyond the interest in understanding
how lignocellulose is broken down, though, he says, “overall we’re
getting to the point where we can do comparisons across the three fungal
lifestyles: saprotrophs, which include wood-degraders, symbionts, and
pathogens, and we are entering the stage where we find that there are no
clear, black, and white associations with each category.”
Co-senior
author Francis Martin from the French National Institute of Agriculture
Research (INRA) who has been an integral driver in many of the DOE
JGI’s fungal genome projects, stressed the importance of this work in
understanding the evolution of forest fungi.
“Serpula
is the ‘missing link’ along the ‘saprotrophism-mutualism continuum,'”
Martin says. “Both the brown rot Serpula and symbiont Laccaria
bicolor—also sequenced by the DOE JGI—lack the most aggressive
wood-degrading enzymes used by white rot fungi in breaking down the
unusable lignin matrix of wood to unmask useable cellulose embedded
within it. Loss of this aggressive lignin breakdown mechanism might have
permitted brown rot’s transition to mycorrhizal mutualists—that foster a
beneficial association between the fungus and the plant roots—enabling
preferential access to carbohydrates within the tree.”
This
study, Martin concludes, “adds to our incremental understanding of the
rise of these processes, particularly as they relate to tree health and
productivity, which play pivotal roles in terrestrial carbon cycling,
sequestration, and other biogeochemical cycles, as well as for informing
new strategies for biomass deconstruction for improved biofuels.”
The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi