NEWSFOCUS

Whats inside? Buildings are ecosystems in their

own right and are now being studied as such.

The microbial ecology of buildings gets a boost from a foundation

and researchers trying to better understand the invisible
communities in our homes, hospitals, and workspaces
UNTIL 3 YEARS AGO, NOAH FIERER WAS
Fierer and Dunn plan to compile simiyour typical microbial ecologist. At the Uni- lar microbial survey data from the homes
versity of Colorado, Boulder, he focused on of thousands of volunteers like myself from
the outdoors, studying the microbes inhabit- different parts of the world. The pair wants
ing soils and leaf litter. Then he tackled eco- to explore whether the microbial makeup
logical questions closer to homerst in the of homes differs depending on location, the
microbes living in humans and next in mun- density of the surrounding population, or
dane places like computer keyboards. After whether a home is freestanding or an apartrealizing how much time he spends indoors, ment. It will be the rst comparison of houses
he began thinking bigger. While many sci- from a wide geographic range.
entists have counted the germs on indoor
This basic Lewis and Clark explorasurfaces, few had systematically tried to tion will offer new information. But the
assess the biodiversity of interior spaces. He real goal, Dunn says, is to understand not
and Rob Dunn, an ecologist at North Caro- just what is there but why, and to see the
lina State University in Raleigh,
extent to which these species are
have just mounted a large citizenassociated with our lifestyles,
science survey to do just that.
geography, and climate.
sciencemag.org
Volunteering to be its rst parWhile some scientists worry
Podcast with
ticipant, I rubbed 10 cotton-tipped
that such efforts may simply lead
author Courtney
Humphries.
swabs along surfaces of my apartto meaningless lists of microbes,
mentincluding my door sills,
new information is pouring in
toilet, pillowcase, and countersand sent about the microbial denizens of other kinds
them back to Fierer for DNA sequencing. His of buildings as well. In work that blends
analysis showed that my home hosts a wide microbial ecology, indoor air science, and
variety of microbes.
building engineering, researchers have
Hardy Acinetobacter are burrowed into begun scouring classrooms, ofces, and hosthe crevices of my cutting boards. Counter- pitals for microbial life and analyzing the
tops are biodiversity hot spots of bacteria factors that affect human exposure to it.
and fungi, including sphingomonads that
So far, most of this work on indoor micromay have settled out of the tap water used bial ecology has been funded by the Alfred
to wipe the counter. The toilet seat is coated P. Sloan Foundation, not by the U.S. or other
with bacteria associated with human skin, governments. Since 2004, the foundation has
and doorsills are crawling with fungi and spent more than $23 million on dozens of
grass pollen. The front doorknob and TV such research projects. While novel molecuscreen harbor unusual bacteria not typi- lar techniques have made it possible to study
cally found in water, soil, or the human microbes in many environments, the interibodyperhaps representing entirely new ors of buildings rarely drew the attention of
communities unique to those surfaces.
microbial ecologists, says Sloan Program

Online

648

10 FEBRUARY 2012

VOL 335 SCIENCE www.sciencemag.org

Published by AAAS

CREDIT: JESSICA GREEN

Indoor Ecosystems

A needed eld
The 2001 National Human Activity Pattern
Survey estimated that people in the developed world spend nearly 90% of their time
indoors; yet so much funding and effort goes
into thinking about ecosystems in which we
spend 10% of our time, complains Jessica
Green, a microbiologist at the University
of Oregon, Eugene. She heads the Biology
and the Built Environment (BioBE) Center,
which was created in 2010 with a $1.8 million
grant from the Sloan Foundation.
There are certainly health reasons to pay
more attention to the microbes inside our
buildings. The air circulated by heaters and
air conditioners can spread infectious diseases, for example, and some cases of socalled sick building syndrome can stem from
unchecked mold. Fungi in buildings are also
associated with allergies, asthma, and other
pulmonary conditions.
And then theres the impact on the edices
themselves. Microbes contribute to the deterioration of buildings by breaking down wood,
stone, concrete, and other materials.
Yet little is known about what microbes
live in buildings and why they reside in certain places but not others. As a result, homeowners and building managers who invest
time, money, and energy cleaning surfaces
and ltering air do not really know the effects
of these activities. Choices in construction materials, ventilation systems, building
design, and maintenance also inuence an
interiors microbial complement, but how?
In order to understand what shapes the
diversity and function of microbes indoors,
you must understand the indoor environment
from an abiotic contextits chemistry, structure, and dynamics, Green says.
Greens background provides her with a
strong appreciation of the need to blend abiotic and biotic factors. She began her studies in civil engineering and earned a Ph.D. in
nuclear engineering, but eventually switched
to microbial ecology because of a passion for
biodiversity. Before coming to Oregon, she
had focused on microbial diversity in soils
and oceans. But attracted to the universitys
program in sustainable building design and
inspired by the potential of Sloan support, she
joined forces with two university colleagues,

Downloaded from www.sciencemag.org on February 10, 2012

Director Paula Olsiewski. At the same time,

building scientists were assessing chemicals and particles in indoor air but ignoring
its biology. We thought it was important to
study where people live, Olsiewski says.

NEWSFOCUS

Anybody home?
To help them take that next step, Fierer and
others in the eld turn to software programs
that help match the microbial DNA sequences
from their surveys with known bacteria and the
other environments in which those microbes
have been found. As genome sequencing costs
have come down, the databases of microbial
DNA have exploded. These resources help
researchers track whether microbes that live
indoors come from soil, outside air, humans,
other animal occupants, or some other source.
Using these databases, Fierers group
recently identified the probable sources of
microbes from several surfaces in 12 public bathrooms. The results, published on
23 November 2011 in PLoS ONE, were not
surprising: Bacteria associated with human
skin abound on surfaces people touch; bacteria from the gut occupy toilet seats; and a
higher level of vaginal microbes was found

in womens bathrooms than mens. But Fierer

says the study shows its possible to see spatial patterns in the origins of microbes, and his
team is now working on a project to create a
detailed atlas of the typical spatial patterns of
microbes found in kitchens.
For Greens latest project, she and her colleagues conducted a classical ecological study
on the microbial diversity in one University
of Oregon building. Similar to how Green
and others have examined microbes in natural environments, the researchers repeatedly
took samples from the building, hoping to
provide enough data to make inferences about
the causes and consequences of microbial
diversity indoors. For example, they collected
air from six rooms at different times of the
day to understand the dynamics of microbes
over time and their response to human presence. They also gathered dust from each of
the buildings more than 300 rooms to understand how microbial populations vary across

Microbe collector. Jessica Green is applying ecological methods and theory to indoor spaces.

www.sciencemag.org SCIENCE VOL 335

Published by AAAS

Systematic study. Researchers collected microbes

from air (left, middle) and surfaces (right) in a campus building to understand its microbial ecology.

Downloaded from www.sciencemag.org on February 10, 2012

CREDITS: (TOP LEFT TO RIGHT) ANGIE PONSO; JESSICA GREEN (2); (BOTTOM) ANGIE PONSO

microbiologist Brendan Bohannan and architect G. Z. Charlie Brown, to launch BioBE.

Because indoor ecology is an emerging eld, Green and other researchers must
struggle with developing effective protocols
for assessing these ecosystems and nding
practical applications for their insights. For
example, Fierer and Dunn are taking steps
to standardize their citizen-science microbial
survey; theyll place extra weight on samples
from a core set of participantsincluding
other scientistswho will provide more indepth data by sampling the same spots several
times. Fierer and Dunn hope to identify reproducible patterns in their results that will yield
real insights into what factors determine the
microbial residents, rather than just a census.
Thats my criticism of the field, that
youre just getting a list, says Jordan Peccia,
an environmental engineer at Yale University
who studies how moving air affects microbes
in buildings. But, Fierer counters, without
that basic knowledge, its hard to take the
next step.

an entire building. To study the microbial variability within individual rooms, Greens team
chose different habitatsfloors, walls,
desktops, and seatsand used square sample
plots set up the same way as those historically
used to study plant biodiversity.
The analysis by the Oregon group is
ongoing, but part of the goal is to model relationships between building use and design
and microbial diversity. The team is also trying to discover whether ecological theories
developed from studying plant and animal
diversity on islands, a well-researched topic,
can help them make sense of the ecology of
microbes indoors.
You can think of a building as a collection of islands, Bohannan says. Although
individual rooms are somewhat self-contained environments, like islands are, they are
linked through ventilation and the movement
of occupants. If this island model turns out to
be true, Bohannan says, it would mean that the
movement of microbes between rooms affects
their ecology as much as the conditions of the
room, and building design and management
could be manipulated to control this dispersal.
Moving air moves microbes
Green and Bohannan have already begun
to look at how ventilation affects indoor
microbes. Over the past few decades, the
push to reduce energy use has created buildings that are highly sealed to outside air, and
the Oregon researchers are trying to understand the consequences of this reduced air
exchange. To do that, Greens team recently
turned to an Oregon hospital, because hospitals typically have ventilation that is tightly
controlled. They initially surveyed the microorganisms in mechanically ventilated rooms
with windows closed and repeated the census
after opening the rooms windows for 2 hours.

10 FEBRUARY 2012

649

NEWSFOCUS
100

SOURCES

Average contribution (%)

Soil

80

Water
Mouth
Urine

60

Gut
Skin

40
20
0

10 FEBRUARY 2012

pant in indoor microbial

ecology research, Peccia
thinks that the field has
yet to gel. And the Sloan
Foundations Olsiewski
shares some of his concern. Everybodys generating vast amounts of
data, she says, but looking across data sets
can be difcult because groups choose different analytical tools. With Sloan support,
though, a data archive and integrated analytical tools are in the works.
To foster collaborations between microbiologists, architects, and building scientists,
the foundation also sponsored a symposium
on the microbiome of the built environment
at the 2011 Indoor Air conference in Austin,
Texas, and launched a Web site, MicroBE.net,
thats a clearinghouse of information on the
eld. Although Olsiewski wont say how long
the foundation will fund its indoor microbial
ecology program, she says Sloan is committed
to supporting all of the current projects for the
next few years. The programs ultimate goal,
she says, is to create a new eld of scientic
inquiry that eventually will be funded by traditional government funding agencies focused
on basic biology and environmental policy.
Matthew Kane, a microbial ecologist and
program director at the U.S. National Science Foundation (NSF), says that although
there was interest in these questions prior
to the Sloan program, the Sloan Foundation
has taken a directed approach to funding
the research, and I have no doubt that their
investment is going to reap great returns. So
far, though, NSF has funded only one study
on indoor microbes: a study of Pseudomonas
bacteria in human households.
As studies like Greens building ecology
analysis progress, they should shed light on
how indoor environments differ from those
traditionally studied by microbial ecologists.
Its important to have a quantitative understanding of how building design impacts
microbial communities indoors, and how
these communities impact human health,
Green says. But it remains to be seen whether
well someday design and maintain our buildings with microbes in mind.
COURTNEY HUMPHRIES

Courtney Humphries is a freelance writer in Boston and

author of Superdove.

VOL 335 SCIENCE www.sciencemag.org

Published by AAAS

Downloaded from www.sciencemag.org on February 10, 2012

CREDITS (TOP TO BOTTOM): (PHOTO) COURTESY GILBERTO FLORES; (CHART) G. E. FLORES ET AL., PLOS ONE 6, 11 (2011); PHOTO BY SISIRA GORTHALA

they move around. But to quantify those contributions, Peccias team has had to develop
new methods to collect airborne bacteria and
extract their DNA, as the microbes are much
less abundant in air than on surfaces.
In one recent study, they used air lters
to sample airborne particles and microbes
in a classroom during 4 days during which
students were present and 4 days during
which the room was vacant. They measured
the abundance and type of fungal and bacterial genomes present and estimated the
microbes concentrations in the entire room.
By accounting for bacteria entering and leaving the room through ventilation,
they calculated that people shed
or resuspended about 35 million
bacterial cells per person per hour.
That number is much higher than
the several-hundred-thousand
maximum previously estimated
to be present in indoor air, Peccia
reported last fall at the American
Association for Aerosol Research
Conference in Orlando, Florida.
His groups data also suggest
that rooms have memories of
past human inhabitants. By kicking into the air settled microbes
from the oor, occupants expose
themselves not just to the
microbes of a person coughing
next to them, but also possibly to
Outside inuence. Students prepare to sample air outside a class- those from a person who coughed
in the room a few hours or even
room in China as part of an indoor ecology study.
days ago.
physics of aerosols to look more closely at
Peccia hopes to come up with ways to
how the movement of air affects microbes. describe the distribution of bacteria indoors
Peccia says his group is building on work by that can be used in conjunction with existair-quality engineers and scientists, but we ing knowledge about particulate matter and
want to add biology to the equation.
chemicals in designing healthier buildings.
Bacteria in air behave like other particles; My hope is that we can bring this enough to
their size dictates how they disperse or settle. the forefront that people who do aerosol sciHumans in a room not only shed microbes ence will nd it as important to know biology
from their skin and mouths, but they also as to know physics and chemistry, he says.
drum up microbial material from the oor as
Still, even though hes a willing partici-

650

Bathroom biogeography. By
swabbing different surfaces in
public restrooms, researchers
determined that microbes vary in
where they come from depending on the surface (chart).

Do
or
Do in
or
ou
t
St
all
i
Fa Sta n
uc
et ll ou
So han t
ap
d
dis les
pe
ns
To
T
e
ile oile r
tf
t
lus sea
hh t
a
To ndle
ile
tf
lo
Si or
nk
flo
or

In just that short time, the

microbes had begun to take
on a signature of outside
air (more types from plants
and soil), and 2 hours after
the windows were shut
again, the proportion of
microbes from the human
body increased back to previous levels.
T h e s t u d y, wh i c h
appeared online 26 January in The ISME Journal,
found that mechanically
ventilated rooms had lower
microbial diversity than ones with open windows. The availability of fresh air translated
into lower proportions of microbes associated with the human body, and consequently,
fewer potential pathogens. Although this
result suggests that having natural airow
may be healthier, Green says answering that
question requires clinical data; shes hoping
to convince a hospital to participate in a study
to see if the incidence of hospital-acquired
infections is associated with a rooms microbial community.
For his part, Peccia, who is also a Sloan
grantee, is merging microbiology and the