Plant microbiomes—an introduction
Just like humans, plants have recently been recognized as meta-organisms, possessing
a distinct microbiome and revealing close symbiotic relationships with their associated
microorganisms (Berg et al., 2013; Mendes et al., 2013). Each plant harbor specific
species to a certain degree but also cosmopolitan and ubiquitous microbial strains;
the majority of them fulfill important host as well as ecosystem functions (rev. in
Berg and Smalla, 2009). In addition to the microbe-rich rhizosphere, which has been
studied extensively, the phyllosphere is of special interest for the study of indoor
microbiomes due to its large and exposed surface area and its remarkable microbial
diversity (Lindow and Leveau, 2002; Lindow and Brandl, 2003; Redford et al., 2010;
Meyer and Leveau, 2012; Vorholt, 2012; Rastogi et al., 2013). In addition to the majority
of beneficial and neutral inhabitants, all plant-associated microbiomes contain plant
as well as human pathogens (Berg et al., 2005; Mendes et al., 2013). A broad spectrum
of plant pathogens is well-known from disease outbreaks. Human pathogens belong mainly
to the so called opportunistic or facultative human pathogens such as Burkholderia
cepacia, Pseudomonas aeruginosa or Stenotrophomonas maltophilia, which cause diseases
only in patients with predisposition or in hospital (Berg et al., 2005; Ryan et al.,
2009).
Microbiomes of humans and plants are currently intensively studied using the same
methods and addressing similar scientific questions (Ramírez-Puebla et al., 2013).
However, knowledge about the microbiomes' interaction, microbial dynamics and exchange
in a certain biotope or even indoor environment is very much limited. Although the
composition and function of plant microbiomes is well-studied, there is still little
to no information regarding their overlap, interaction with -and impact on other microbiomes
or the microbiome-harboring hosts. Information is available about the connection of
soil and rhizosphere microbial diversity, which share a selective sub-set (Smalla
et al., 2001). The root-soil interface is the selection site for plant-associated
bacteria by root exudates, which acts as chemo-attractants as well as repellents to
which bacteria respond (Badri and Vivanco, 2009). In addition, plant defense signaling
play a role in this process (Doornbos et al., 2012). For the phyllosphere we know
that there is only a part of residents, while a substantial part of bacteria is shared
with the air microbiome (Lindow and Brandl, 2003). Based on these data, a strong interaction
and exchange of rhizosphere and phyllosphere microbiomes with other microbiomes is
obvious. However, this opinion paper focuses on the question, if there is also a connection
from plant–to indoor microbiomes as well as an impact on human health.
Indoor microbiomes— importance and origin
Despite the fact that the majority of our lifetime is spent in indoor environments
such as home, work place, or public buildings, our knowledge of microbial diversity
inside buildings is limited. We are not alone in these indoor environments: they provide
new habitats and residence to numerous microbial communities comprising possibly hundreds
of individual bacterial, archaeal and fungal species including diverse viruses. Recent
studies analyzed potentially pathogenic and allergenic indoor microorganisms with
mainly cultivation-based methods (Täubel et al., 2009; Yamamoto et al., 2011). Since
the fraction of cultivable microbes on one specific medium is extremely low, information
about specifically-adapted micro-organisms, or those with special needs, remains inaccessible
by standard cultivation assays. Recently, however, the application of molecular methods,
including next generation sequencing (NGS) techniques has provided new insights into
indoor microbial communities, revealing a generally high prokaryotic diversity including
diverse bacterial, archaeal and fungal phyla (Flores et al., 2011, 2013; Moissl-Eichinger,
2011; Hewitt et al., 2012, 2013; Kembel et al., 2012; Dunn et al., 2013; Kelley and
Gilbert, 2013; Meadow et al., 2013).
Indoor microbial communities are an important component of everyday human health (Arundel
et al., 1986; Lee et al., 2007; Kembel et al., 2012). Due to human activity and high
emission rate of up to 106 bacteria per person-hour as measured via 16S rRNA gene
quantification from aerosols (Qian et al., 2012), indoor environments are strongly
influenced by typically human-associated bacteria (Fierer et al., 2008). Hence, built
environments like hospitals are more easily colonized to a large extent by patient-associated
microbes (Oberauner et al., 2013). As a result, many patients in hospitals and especially
in intensive care units (ICUs) develop hospital-acquired “nosocomial infections” that
compound their underlying severe disease (Vincent et al., 1995; Plowman, 2000). Moreover,
these nosocomial infections remain among the leading causes of death in developed
country hospitals. The risk to get nosocomial infections for patients in European
ICUs was reported as 45% (Plowman, 2000). Hospital surfaces are often overlooked reservoirs
for these bacteria (Hota, 2004; Gastmeier et al., 2005; Kramer et al., 2006). Apart
from hospitals, indoor microorganisms affect human health as allergenic agents as
well (Hanski et al., 2012). Indoor microorganisms are also involved in the development
of the Sick Building Syndrome (SBS), which causes symptoms such as sensory irritation
of the eyes, nose, and throat, neurotoxic or general health problems, skin irritation,
non-specific hypersensitivity reactions, and odor and taste sensations (Godish, 2001).
Indoor microbiomes originate primarily from human skin, pets, or the outside air (Flores
et al., 2011; Kembel et al., 2012; Meadow et al., 2013). Plants as a source of indoor
microbes are so far less considered. However, air-borne microbes as substantial part—bacteria,
fungi or microscopic algae—are scattered and can travel long distances such as in
the wind or in clouds before returning to ground-level (Hamilton and Lenton, 1998).
They have received more attention because they can serve as nuclei for condensation
and as such influence our world climate as rain-making bacteria. Interestingly, cloud
and hailstone studies indicated plant-surface bacteria as the dominant source of these
rain-making microbes (Morris et al., 2008; Šantl-Temkiv et al., 2013). In addition,
little is known about the impact of houseplants and its microbes, although older studies
indicate indoor plants as important source (Burge et al., 1982).
Comparing indoor with plant microbiomes, it is our opinion that both outside and inside
plants are of importance for our indoor microbiome. Plants provide beneficial bacteria
for indoor rooms and therefore can positively influence human health. The following
facts support our opinion about the importance of plants as source for a beneficial
microbial biodiversity:
Empirically the positive effects of houseplants and flowers are well-known, but there
is also evidence for psychological effects such as stress reduction and creative task
performance (Fjeld et al., 1998; Shibata and Suzuki, 2004; Chang and Chen, 2005; Bringslimark
et al., 2007; Dijkstra et al., 2008). In addition houseplants feature a remarkable
capacity to improve indoor air quality (Orwell et al., 2004). This melioration of
indoor air is not only due to the filtering capacity of plant leaves, but also by
the degrading effects of their root associated microbes (Pegas et al., 2012 up to
90% formaldehyde removal during night according to Kim et al., 2008).
Plant DNA as frequently detected as chloroplast 16S rRNA gene sequences in amplicon
surveys is a substantial part of all indoor microbiomes, but mainly filtered out for
the presentation of data (Oberauner et al., 2013). This emphasizes, that pollen and
seeds of plants, which are densely colonized by bacteria (Fürnkranz et al., 2012)
are dispersed into the indoor environment and thus provide excellent shuttles for
microbiome exchange.
Typical and often dominant plant-associated bacteria are members of the indoor microbiome.
A relationship of bacteria genera occurring on plants and indoors is given in Figure
1. There are many ways for plant microbes to enter the built environment; as already
mentioned on pollen, seeds, fog, soil on shoes, flowers, fruits and vegetables as
well as transmitted by animals and other visitors.
At species level, no differentiation was possible for clinical and plant-associated
isolates. This was studied for Burkholderia cepacia, Pseudomonas aeruginosa and Stenotrophomonas
maltophilia (Ryan et al., 2009; Martins et al., 2013). Unfortunately, these plant-associated
bacteria can infect immuno-compromised patients with high predisposition in hospitals.
On the one hand this is an evidence for the interplay of the plant and indoor microbiome,
but on the other hand it highlights the beneficial balance, which is necessary between
microorganisms and hosts.
Interestingly, Thaumarchaeota, originally described to be associated with ammonia-oxidation
in soil and the rhizosphere of plants, have been found on human skin (Probst et al.,
2013). Currently it is unknown, whether the human skin archaea have positive or negative
effect on human health and whether they have different genomic capabilities compared
to their soil-relatives. However, it becomes clear, that closely related microorganisms
can exist in different microbiomes, based on a dynamic exchange or distribution and
subsequent development of adaptation strategies.
Figure 1
Relationships between the plant and indoor microbiome. The indoor microbiomes, influenced
by transmissions via air, soil, food, houseplants and animals from plant microbiomes,
presents an overview on typical and dominant bacterial groups occurring in the built
environment. Schematic chart represents occurrence of the bacterial inhabitants indoors.
Bacterial families and genera (white ellipses) are arranged according to their phylum
affiliation (bold) and are connected to certain types of the built environments (red
squares). Taxa highlighted in green are typical phyla detectable in plant microbiomes.
This image has no demand of being complete.
Based on these facts, we speculate the following:
Enclosed environments and their microbiomes—like private/public buildings, hospitals,
and clean rooms, which are more or less separated from outside, are especially shaped
by human influence and human associated microbes (Hospodsky et al., 2012; Dunn et
al., 2013). Hence, microbial diversity is altered and partially reduced compared to
the outdoor environment. A reduction in microbial diversity is well known to facilitate
dominant proliferations of certain strains, which might bear the risk to have a negative
effect toward our health. To increase microbial diversity in an indoor environment
we could simply open our windows instead of using air-condition (Hanski et al., 2012;
Kembel et al., 2012; Meadow et al., 2013). Alternatively, we could use potted houseplants
in built environments as a source of microbial biodiversity and possibly beneficial
microorganisms.
Microbes, which live in close vicinity to human beings, are adapted to us as symbionts,
commensals, or pathogens, whereas these life-styles are changeable dependent on the
host-microbe balance. Indoors we share these microbes, which might get deposited on
various surfaces by one person and afterwards get collected by another. Human-associated
microbes e.g., skin associated, are confronted with totally new biotic and abiotic
factors in the built environment. Here they have to adapt to new surface materials,
compete with others for scarce nutrients and withstand stresses associated to cleaning
reagents etc. However, in the case of houseplants we allow them to proliferate in
a protected environment. Plant associated microbes stay on the leave or stem surface,
where they have adapted to and are sheltered from cleaning procedures. Although these
phyllosphere communities are confronted with an absence of direct sun light and rain
as well as other changed meteorological parameters like air/dust turbulences, their
rhizosphere and surrounding soil communities stay in their natural habitat. Hence,
these well balanced plant communities, which we bring inside, have the potential to
balance an indoor microbiome, by increasing its diversity and filter airborne microbes.
Conclusion
Members of the plant microbiome are an important source for indoor microbiomes. Both,
plants from inside and outside can contribute to the micro-flora. Plant-associated
bacteria could act as counterparts against pathogens within the microbial ecosystems.
They stabilize the ecosystem, enhance biodiversity and avoid outbreaks of pathogens.
However, more research is necessary to understand the microbiology of indoor environments.
Currently used cleaning and hygiene strategies in built environments especially in
hospitals and ICUs often promote multi-resistant pathogens instead of supporting beneficials.
In future, it is important to re-think our understanding of necessary sterility and
our relationship to our surrounding microbiomes. This “paradigm shift in ecology”
is not only required for plants, humans (Jones, 2013) but also for our environment.
Fortunately, “omics”-technologies guided by next-generation sequencing and microscopic
techniques allow us now a much better assessment of them. Moreover, we can develop
management strategies for beneficial interactions.