Other host filters can be very specific constraints including constitutive secretion of
antimicrobial compounds and adaptive immunity. Constitutive chemicals are common in the marine environment, such as antimicrobial peptides in the arminin
family, produced by Hydra species and resulting in low bacterial diversity and
abundance (Franzenburg et al. 2013) or halogenated furanones, produced by red
algae that interfere with cell signaling in bacteria (Longford et al. 2019). Physical
filters have received less attention, but can be important in maintaining a core
microbiome. For example, the proventriculus is a microporous (0.2 μm) valve that
acts as a bacterially restrictive filter controlling movement between the crop and the
midgut of some insects, including the Sonoran desert turtle ant (Cephalotes rowheri)
(Lanan et al. 2016). Another example of physical filters can be found in the Bobtail
Squid (Euprymna scolopes) using ciliary action to control water flow on the surface
of the luminous organs creating an extreme type of biological filter that can exclude
all but one bacterial species, V. fisheri (Nyholm and McFall-Ngai 2004). Other hosts
are able to distinguish between resident microbiota and foreign invaders. Adaptive
immunity in humans includes a dynamic molecular dialog with resident microbiota
that seems to allow for discriminatory responses to pathogens and foreign microbes
(Lee and Mazmanian 2010). Most host filters reduce diversity by constraining which
species are recruited to their tissues, while ultimately increasing microbial function
in terms of host fitness benefits.
In fact, failure of host control via habitat filters can result in disease and reduced
fitness. For example, human skin is a dry, salty environment, full of sebaceous
glands, and characterized by variations in temperature that favor typical skin bacteria
like Staphylococcus spp. (Chen and Tsao 2013; Oh et al. 2016). Atopic dermatitis
occurs when the host fails to produce the epithelial barrier protein filaggrin, inducing
changes in the skin microbiome that include colonization and proliferation by
S. aureus and other pathogens with an associated immune response (Chen and
Tsao 2013). Similarly, disease in the corals Porites astreoides (Meyer et al. 2014),
and Montastrea lanceolata (Sunagawa et al. 2009) are associated with increased
bacterial diversity. In contrast, other types of disease or dysbiosis are associated with
reduced diversity which can be explained by the proliferation of dominant taxa that
outcompete beneficial microbes. For example, the gut parasite Crithidia reduces
richness and abundance of core taxa in the bumblebee (Cariveau et al. 2014).
Other host habitats are permissive to microbial colonization without resulting in
disease. Even when receiving colonists from other hosts and the surrounding
environment, these communities’ diversity and function can be under the control
of microbe–microbe interactions that limit invasion by pathogens and cheaters.
Some habitats open to colonization are strongly dependent on early arrival of
colonists that monopolize resources and space, a mechanism known as priority
effects. Flower nectar microbes, known for their influence in pollination, are a
model system for priority effects, where bacterial early arrival constrains yeast
recruitment and yeast early arrival lowers the pH and limits bacterial recruitment
(Vannette and Fukami 2017; Toju et al. 2018). Priority effects may be common in
other systems, such as seaweed surface bacteria, where the order of arrival follows a
lottery model (taxa arrive randomly at new sites and early recruits monopolize
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antimicrobial compounds and adaptive immunity. Constitutive chemicals are common in the marine environment, such as antimicrobial peptides in the arminin
family, produced by Hydra species and resulting in low bacterial diversity and
abundance (Franzenburg et al. 2013) or halogenated furanones, produced by red
algae that interfere with cell signaling in bacteria (Longford et al. 2019). Physical
filters have received less attention, but can be important in maintaining a core
microbiome. For example, the proventriculus is a microporous (0.2 μm) valve that
acts as a bacterially restrictive filter controlling movement between the crop and the
midgut of some insects, including the Sonoran desert turtle ant (Cephalotes rowheri)
(Lanan et al. 2016). Another example of physical filters can be found in the Bobtail
Squid (Euprymna scolopes) using ciliary action to control water flow on the surface
of the luminous organs creating an extreme type of biological filter that can exclude
all but one bacterial species, V. fisheri (Nyholm and McFall-Ngai 2004). Other hosts
are able to distinguish between resident microbiota and foreign invaders. Adaptive
immunity in humans includes a dynamic molecular dialog with resident microbiota
that seems to allow for discriminatory responses to pathogens and foreign microbes
(Lee and Mazmanian 2010). Most host filters reduce diversity by constraining which
species are recruited to their tissues, while ultimately increasing microbial function
in terms of host fitness benefits.
In fact, failure of host control via habitat filters can result in disease and reduced
fitness. For example, human skin is a dry, salty environment, full of sebaceous
glands, and characterized by variations in temperature that favor typical skin bacteria
like Staphylococcus spp. (Chen and Tsao 2013; Oh et al. 2016). Atopic dermatitis
occurs when the host fails to produce the epithelial barrier protein filaggrin, inducing
changes in the skin microbiome that include colonization and proliferation by
S. aureus and other pathogens with an associated immune response (Chen and
Tsao 2013). Similarly, disease in the corals Porites astreoides (Meyer et al. 2014),
and Montastrea lanceolata (Sunagawa et al. 2009) are associated with increased
bacterial diversity. In contrast, other types of disease or dysbiosis are associated with
reduced diversity which can be explained by the proliferation of dominant taxa that
outcompete beneficial microbes. For example, the gut parasite Crithidia reduces
richness and abundance of core taxa in the bumblebee (Cariveau et al. 2014).
Other host habitats are permissive to microbial colonization without resulting in
disease. Even when receiving colonists from other hosts and the surrounding
environment, these communities’ diversity and function can be under the control
of microbe–microbe interactions that limit invasion by pathogens and cheaters.
Some habitats open to colonization are strongly dependent on early arrival of
colonists that monopolize resources and space, a mechanism known as priority
effects. Flower nectar microbes, known for their influence in pollination, are a
model system for priority effects, where bacterial early arrival constrains yeast
recruitment and yeast early arrival lowers the pH and limits bacterial recruitment
(Vannette and Fukami 2017; Toju et al. 2018). Priority effects may be common in
other systems, such as seaweed surface bacteria, where the order of arrival follows a
lottery model (taxa arrive randomly at new sites and early recruits monopolize
17 Diversity–Function Relationships and the Underlying Ecological Mechanisms in. . .
313