MtlMICRO: Montreal Microbial Ecology and Evolution Group

January 17th 2018 - Université de Montréal

https://mtlmicrobio.wixsite.com/mtlmicrobiogroup
 Microbiomes and the -omics approach
⇒ Studies in the last decade: microbial communities living in and on eukaryotic
hosts (microbiomes) are of great importance, playing roles in:

- Host phenotype and pathogen susceptibility

- Nutrient acquisition, metabolism and ability to cope with stressful environments

⇒ NGS and metagenomics: move beyond describing culturable species

⇒ Recent move away from describing “who” towards

determining what they are doing: metatranscriptomics and
metabolomics
 Advantages of combining methods to understand microbiome function

a) Detection of genes/pathways that are overexpressed (orange squares) or underexpressed (green triangles)
relative to their sequence abundance
b) Detection of functional redundancy (functional div. reduced relative to taxonomic composition) and
differential expression between healthy (blue) and diseased (yellow) individuals
c) Measure of associations (positive in red, negative in green) between particular taxa and known metabolites
or metabolic pathways
Functional characterization approach
⇒ Extreme end: to shift focus from the organisms making up the microbiota to the
genes making up the microbiome (community function)

Problems with the approach:

⇒ Datasets (both metagenomics and metatranscriptomics) are not easily interpreted

in terms of classical community ecology

Open question: What are the fundamental units of evolution? Genes, traits, or
species/population?
Microbiomes in the face of ecological and evolutionary theories

⇒ A number of unique characteristics of microbial species (e.g. rapid evolution,

HGT) are not easily accommodated by current ecological and evolutionary theory

⇒ A mishmash of timescales

Due to short generation times and small genomes, community processes that are
typically grounded in ecology have increasing overlap with evolution for mic. comm.

Ecology
Changes in spp abundance
Evolution
Changes in gene frequencies
 Discordances relative to theory developed for eukaryotes
1 ⇒ De novo mutations (broadly ignored for eukaryotic systems) are a potential
source of variation during colonization and succession in the microbiome

⇒ Ecological succession: important who arrive first and how competitive they are (r vs.
k strategists)

2 ⇒ Rapid turnover of genes/species within microbiomes confound classic

mechanisms for species coexistence

⇒ Competitive exclusion principle: to coexist species must not directly compete

Sp1 Sp2 Sp1 Sp2

Resource use (niche overlap) Resource use (niche overlap)

~ Hutchinson Paradox of the plankton
⇒ Since microbial communities are in a constant state of flux as a result of fast
and overlapping timescales, competitive exclusion may not have time to play out

⇒ Functional redundancy, the converse of character displacement, seems

widespread in the microbiome

⇒ Predictive factors for coexistence in microbial communities:

- Phylogenetic distance
- Genome similarity
- Functional association among microbes
 Is neutral theory applied to microbiomes?
⇒ Community dynamics governed by dispersal (or mutation) limitation and stochastic
extinction rather than competitive differences

⇒ Evidences for the neutral theory, which should be expected, are so far mixed

⇒ Data suggest that deterministic processes are important in shaping microbiome

BUT THE NUANCE of how these processes operate in the face of shifting timescales
and when/why the neutral theory can be appropriately applied are important
questions for further work
BEYOND adaptation to competitors
⇒ Adaptations against predators and phage are also likely important in
colonization of and success within the microbiome

⇒ The enemy release hypothesis: classical theory suggests that colonists

have an increased chance of establishment because they have left behind
antagonists
BEYOND adaptation to competitors
⇒ Adaptations against predators and phage are also likely important in
colonization of and success within the microbiome

⇒ The enemy release hypothesis: classical theory suggests that colonists

have an increased chance of establishment because they have left behind
antagonists

⇒ No such evidence for microbiota and their phages or predators

AGAIN, fast and overlapping timescales may be important here

The speed at which phage-mediated selection can alter bacterial traits that influence both competition
and interactions with host can further blur the line between ecological and evolutionary timescales
 Ecosystem engineering
⇒ Many microbiome species also considerably alter their environment

⇒ Focus of ecosystem engineering has been on impacts on the abiotic environment

⇒ For the microbiome, the speed at which ecosystem engineering occurs in and
interacts with the biotic environment (including hosts and other microorganisms)
may well be unique
 Ecosystem engineering
⇒ Many microbiome species also considerably alter their environment

⇒ Focus of ecosystem engineering has been on impacts on the abiotic environment

⇒ For the microbiome, the speed at which ecosystem engineering occurs in and
interacts with the biotic environment (including hosts and other microorganisms)
may well be unique
Open questions: How species found in a microbiome will impact
future species colonization?

How does diversity relate to microbiome health? Is there such a

thing as a general ‘dysbiosis’ (i.e. the microbiome composition
associated with a diseased state)?
 A question of identity
⇒ Difficulty for identifying players involved (OTUs/MAGs) by taxonomic, phylogeny, or
function

+ Conceptual and epistemological challenges arise around the question of identity

in the microbiome

⇒ HGT can blur the line between phylogenetic and phenotypic

distance: acquisition of new traits
Functional diversity & the Black Queen Hypothesis
⇒ Microbiota composition was found not to mirror functionality

⇒ Tightly associated-associated bacterial species are likely to rapidly lose genes

that are functionally redundant in the presence of other community members,
potentially due to:

- Relaxed selection
- Genetic drift
- Positive selection (Black Queen hypothesis)

⇒ The BQH predicts that the loss of a costly, leaky function is selectively favored
at the individual level, but may leave organisms dependent on co-occurring
microbes for the lost metabolic functions (Morris et al. 2012, mBio 3(2):e00036-12)
Genes rather than organisms
⇒ Rapid loss of redundant genes/traits + rapid gain of genes through HGT ⇒
focus towards genes making up the microbiome and away from organisms, a
potentially powerful approach

⇒ But raises the challenge in bringing current ecological and evolutionary theory to
the microbiome

Open question: How does the scale at which we describe the microbiome influence
our interpretation?
Blurry heritability and the Holobiont concept
⇒ To which degree are microbiomes heritable?

⇒ Highly heritable microbiome could result in co-selection acting on the

host and microbiome together (the holobiont concept)

Open question: Where does the holobiont begin and end? Permanent or
‘core’ members of the microbiome are more likely to experience co-
selection than transient members. But it shouldn’t also depend on when
are the transient members present? Is the microbiome of pregnant
females somehow different?
Vertical vs. Horizontal transmission
Assess relative importance of vertical vs horizontal
transmission is important to understand the complex role of
heritability in host-microbiome coevolution

⇒ Vertical transmission ⇒ maintain mutualistic interactions

⇒ Horizontal transmission ⇒ can select for more virulent

pathogens

Open question: How much of our microbiome is transmitted,

inherited, or acquired?
 The host control
⇒ In the opposite direction of thinking of host and microbiome together, it is
important to consider another factor that shape microbiomes: the host control

⇒ Microbiomes shape and are shaped by the environment in which they live

⇒ The result is a co-evolutionary process, operating on profoundly different

timescales (hosts >> species within their microbiome), in the context of complex
community interactions and ecosystem engineering within the microbiome

Open question: How do non-bacterial microbiome communities

impact host health and interact with the bacterial microbiome?