Intra- and inter-species interactions in microbial communities

Abstract

In this Special Topic we explore some of the novel mechanisms interconnecting microbes within and across species, and to their physical environment, across vastly different scales. As developments in various “OMICs” fields have revolutionized our understanding of the vast diversity and ubiquity of microbes in the biosphere, we have also developed new holistic ways of thinking about them. Human microbiome scientists are currently thinking about the whole set of microorganisms in the human intestine as a single entity or as one organism (Li, 2014). In the confined environment of the human body and subjected to a tight interaction with the host, this conceptual shift from individual microbes and “species” to their integrated set of inputs and outputs may seem natural. Individual microbes react individually tothehostenvironmentinthecontextofothermicrobesandtheir mutual interactions, producing as a result an integrated collective behavior. The human body in turn processes and reacts to this aggregated result, the behavior and actions of the whole microbial community. Thus, while individual bacteria interactions occur at the nanoscale size range, bacterial communities are shaped by landscape structures from the microscale or larger and produce collective behavior at such a scale as well.

Full text

EDITORIAL
published: 24 November 2014
doi: 10.3389/fmicb.2014.00629
Intra- and inter-species interactions in microbial
communities
Luis R. Comolli*
Beamline 4.2.2, Advanced Light Source, ALS-Molecular Biology Consortium, Berkeley, CA, USA
*Correspondence: lrcomolli@gmail.com
Edited by:
Lisa Y. Stein, University of Alberta, Canada
Reviewed by:
Jay T. Lennon, Indiana University, USA
Keywords: archaea, microbial communities, inter-species interactions, uncultivated biofilms, microbial networks
In this Special Topic we explore some of the novel mechanisms
interconnecting microbes within and across species, and to their
physical environment, across vastly different scales.
As developments in various “OMICs” fields have revolution-
ized our understanding of the vast diversity and ubiquity of
microbes in the biosphere, we have also developed new holistic
ways of thinking about them. Human microbiome scientists are
currently thinking about the whole set of microorganisms in the
human intestine as a single entity or as one organism (Li, 2014).
In the confined environment of the human body and subjected to
a tight interaction with the host, this conceptual shift from indi-
vidual microbes and “species” to their integrated set of inputs and
outputs may seem natural. Individual microbes react individually
tothehostenvironmentinthecontextofothermicrobesandtheir
mutual interactions, producing as a result an integrated collective
behavior. The human body in turn processes and reacts to this
aggregated result, the behavior and actions of the whole microbial
community. Thus, while individual bacteria interactions occur at
the nanoscale size range, bacterial communities are shaped by
landscape structures from the microscale or larger and produce
collective behavior at such a scale as well.
More open systems are potentially more complex, at least in
terms of having variable or open physical boundaries and a less
tightly regulated dynamic range of local properties. Nonetheless,
across a wide range of diverse environments (soils, lakes, coral
riffs, hot and acidic extreme environments, subsurface aquifers,
and living organisms from plants to animals), whole popula-
tions of microorganisms have developed system-wide homeo-
static adaptations to external factors (Fernandez et al., 2014
and references therein; Karatan and Watnick, 2009). The chem-
ical transmissions of information underlying collective behaviors
such as in quorum sensing have been recognized for a long time
(Ryan and Dow, 2008 and references therein), but we are refer-
ring here to more intimate relationships. In the case of biofilms
it is natural to compare them with tissues (Hall-Stoodley et al.,
2004; Karatan and Watnick, 2009; Subbiahdoss et al., 2009), with
various cell types and the extracellular substances as a matrix
holding the whole together. Genomics data increasingly point
toward the co-existence of metabolically incomplete individual
“species” across environments, including microorganisms within
planktonic systems such as subsurface aquifers (Wri ghto n et al . ,
2012; Castelle et al., 2013). There seems to be a wide range of
phenomena beyond the use of chemical signals to synchronize
behavior across entire populations.
The type and extent of microbe-microbe and microbe-host
nutritional interactions will determine the metabolism of the
entire community in a given environment. We would expect the
choice between biofilm formation and planktonic growth to be
accurately regulated. Indeed, Rajeev et al. (2014) report on two
diguanylate cyclases (DGCs) in the bacterium Desulfovibrio vul-
garis Hildenborough that function as part of two-component
signaling pathway, each one specific for one choice of growth
fate. Once the fate has been committed, the type of interactions,
topological relationships and constraints, and the physical means
to establish them determine metabolic strategies. Nutrient shar-
ing and electron transfer among microbes are reviewed by Seth
and Taga (2014),andShrestha and Rotaru (2014),respectively.
Microbial community members can also gather energy cooper-
atively, from chemical reactions no single species can catalyze.
Two types of electron transfer between microorganisms are rec-
ognized: the transfer of chemical intermediate in redox reactions
and direct electron transfer. These and possibly other modes of
nutrient and energy sharing between microbes are just starting to
be investigated through mechanistic and structural studies.
The physical means used by microbes to form networks or
affect other microbes at a distance are surprising and somewhat
counter-intuitive within old paradigms of species. Perras et al.
(2014) examined uncultivated biofilms taken directly from a nat-
ural sulfidic marsh (Sippenauer Moor near Regensburg, Bavaria,
Germany) by transmission and scanning electron microscopy
(TEM and SEM). The dominant SM1 Euryarchaeon uses thin
appendages to connect to other cells of the same species form-
ing a network in which each cell has an average of six con-
nections, but also connects to cells of other species. In fact,
the archaeal cells appear to connect to bacteria, establishing an
interaction across two kingdoms of life. Comolli and Banfield
(2014) linked cryogenic TEM with genomics and proteomics to
show a range of physical interactions and connections between
archaeal cells of different species, including “synapse-like” and
tubular connections through cell wall openings. The inner diam-
eters of some of these connections are large enough to enable
the exchange of the largest cytoplasmic macromolecules and
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Comolli Intra- and inter-species interactions in microbial communities
molecular machines. Berleman et al. (2014) used conventional
TEM, Mass Spectrometry analysis and biochemistry to investi-
gate outer membrane vesicles (OMV) produced by Myxococcus
xanthus, a bacterial micro-predator known for hunting other
microbes. They analyzed the protein and small molecule cargo
of OMVs conclusively proving that they are associated with
antibiotic activity, including the product of gene mepA, an M36
protease homolog. Taken together these three contributions show
physical means used by microbes to affect other microbes within
their environment but at a distance: how they establish vast
networks with new physical properties than those of individ-
ual microbes; how they interconnect across species physically, in
principle enabling the exchange of gene products; and releasing
enzymatic cargo.
Given a set of experimental observations, models allow us to
explore the minimal set of rules and relationships that could
account for the data; numerical simulations and models also serve
to generate new hypothesis or extend questions beyond the avail-
able experimental data (Silva, 2011). In this Special topic Madeo
et al. (2014) apply game theory in a first model that accounts
for the observed patterns of inter-species interconnections in
imaging data. Sinclair (2014) shows the counter-intuitive pos-
sibility of killer and prey co-existence, an insight of potentially
wide impact. As more extensive imaging data across modalities
shows us patterns and relationships for different types of micro-
bial communities, and highly-resolved metabolomics capabilities
resolving essential co-dependencies are developed, a new gener-
ation of modeling efforts of increasing power and sophistication
will play a key role. New models will likely incorporate dozens
to hundreds of secreted chemicals and metabolites that mod-
ulate the behavior, survival, and differentiation of members of
the community, extending our ability to formulate new testable
hypothesis.
We argue above that microbial communities in defined rela-
tionships or environments should be thought of holistically,
and four papers in this Special Topic do just that. Holmes
and co-authors investigated symbiotic associations of protozoa
and endosymbiotic methanogens in groundwater communities
(Holmes et al., 2014). They show how under certain conditions,
the protozoa hosting endosymbionts become important members
of the microbial community. As they feed on moribund biomass
and produce methane, their system-wide conclusions are rele-
vant for engineered bioremediation approaches in general. Hess
and co-workers (Piao et al., 2014) used 16S rRNA gene profiling
analysis of the cow cellulose-digesting anaerobic rumen ecosys-
tem, where microbial-mediated fermentation degrades a complex
mixture of cellulosic fibers. They show how diverse microbial tax-
onomic groups change in time, such that complete degradation
is the results of their synergistic activity. Gathering an impres-
sive dataset, Freilich and co-authors (Zchori-Fein et al., 2014)
studied variations in the bacterial symbiotic communities of the
sweet potato whitefly Bemisia tabaci (Hemiptera: Aleyrodidae).
Compiling a dataset of over 2000 individuals derived from several
independent screenings, the dataset is unprecedented in num-
ber of individuals as well as the geographical range and habitat
diversity. Their work adds compelling evidence that facultative
endosymbionts complement partial metabolic pathways in the
host, thus modulating their distribution patterns. Guo et al.
(2014) allow us to expand our framework from terrestrial micro-
biology to human oral microbial communities whose synergistic
activities can be pathogenic to us. They surveyed evidence of
cell contact-dependent physical interactions, metabolic interde-
pendencies, and synchronizing signaling systems which are used
to maintain a balanced microbial community but also induce
pathogenic pathways if we do not control them. Mechanisms
conferring robustness, adaptability, and integrated responses are
present in microbial communities from habitats that may seem
inhospitable to us, to microbial communities common in human
environments.
Perhaps conceptual aspects of the “holobiont” play a role at an
entirely more subtle level, as volatile-mediated interactions can
be expected to play an important role in information sharing,
synchronization, and competition among physically separated
microbes. Garbeva et al. (2014) report the first experimental study
indeed proving antibiotic production levels and gene expression
changes in one bacterial species, Pseudomonas fluorescens Pf0-1,
as a consequence of the exposure to volatiles produced by four
different species. In these cases microbes are in direct contact,
confined in a structured space, which they can alter to some
degree, and to which they must adapt too. We can thus rea-
son that these physical aspects inevitably lead to networks and
interactions. However, in the case of microbes distributed in
space at non-obligatory short distances, indeed long variable dis-
tances, the emergence of communications and networks through
volatile chemicals seems to more forcefully challenge the idea of
“single individuals” or “single species.” This work contributes to
expanding how we think of the concept “holobiont.”
Microorganisms with unique positions in the kingdom of life
and the complex web of interactions they participate in are of
great interest, as they can show us either evolutionary remnants or
novel ways to solve the same problems. Lage and Bondoso review
the relatively understudied interactions between Planctomycetes
and macroalgae in the context of complex microbial biofilms
(Lage and Bondoso, 2014). Planctomcyetes share certain features
with archaea, such as proteinaceous cell walls without peptido-
glycan, and some distinctive characteristics with eukaryotes such
as a complex system of endomembranes forming a unique cell
plan. Completing our survey, Ounjai and Chaturongakul review
how bacteriophages affect host gene expression (Chaturongakul
and Ounjai, 2014). As microbes are under evolutionary pres-
sure to improve environmental fitness, bacteriophages need to
dynamically adapt to alter gene expression for their own survival.
Microbes in turn can use part of the bacteriophages machinery
as part of their tool box to compete with other microbes. They
argue that imaging and structural work hold the key to further
elucidating this complex evolutionary relationship.
We have presented a comprehensive survey showing physi-
cal interactions and connections between microbes of different
species, co-occurrence patterns of distribution, and a range of
metabolic interdependencies across environments. As stated in
the opening of this Special Topic, we believe there is a com-
pelling need for imaging data across modalities, providing phys-
ical characterizations linking metagenomics and metaproteomics
to microbial patterns of distribution and networks. We also look
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Comolli Intra- and inter-species interactions in microbial communities
forward for the development of novel imaging instrumentation
and measurement technologies supporting an integrated analysis
of communication among cytoplasmic compartments, between
individual microbial cells, and within multicellular communities
and biofilms.
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Conflict of Interest Statement: The author declares that the research was con-
ducted in the absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Received: 10 October 2014; accepted: 03 November 2014; published online: 24
November 2014.
Citation: Comolli LR (2014) Intra- and inter-species interactions in microbial com-
munities. Front. Microbiol. 5:629. doi: 10.3389/fmicb.2014.00629
This article was submitted to Terrestrial Microbiology,a sect ion ofthe j ournal Frontiers
in Microbiology.
Copyright © 2014 Comolli. This is an open-access article distributed under the terms
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duction in other forums is permitted, provided the original author(s) or licensor are
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