Animals coexist in commensal, pathogenic or mutualistic relationships with complex communities of diverse organisms, including microorganisms1. Some bacteria produce bioactive neurotransmitters that have previously been proposed to modulate nervous system activity and behaviours of their hosts2,3. However, the mechanistic basis of this microbiota-brain signalling and its physiological relevance are largely unknown. Here we show that in Caenorhabditis elegans, the neuromodulator tyramine produced by commensal Providencia bacteria, which colonize the gut, bypasses the requirement for host tyramine biosynthesis and manipulates a host sensory decision. Bacterially produced tyramine is probably converted to octopamine by the host tyramine β-hydroxylase enzyme. Octopamine, in turn, targets the OCTR-1 octopamine receptor on ASH nociceptive neurons to modulate an aversive olfactory response. We identify the genes that are required for tyramine biosynthesis in Providencia, and show that these genes are necessary for the modulation of host behaviour. We further find that C. elegans colonized by Providencia preferentially select these bacteria in food choice assays, and that this selection bias requires bacterially produced tyramine and host octopamine signalling. Our results demonstrate that a neurotransmitter produced by gut bacteria mimics the functions of the cognate host molecule to override host control of a sensory decision, and thereby promotes fitness of both the host and the microorganism.
more »
« less
Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters
Transmitter signalling is the universal chemical language of any nervous system, but little is known about its early evolution. Here, we summarize data about the distribution and functions of neurotransmitter systems in basal metazoans as well as outline hypotheses of their origins. We explore the scenario that neurons arose from genetically different populations of secretory cells capable of volume chemical transmission and integration of behaviours without canonical synapses. The closest representation of this primordial organization is currently found in Placozoa, disk-like animals with the simplest known cell composition but complex behaviours. We propose that injury-related signalling was the evolutionary predecessor for integrative functions of early transmitters such as nitric oxide, ATP, protons, glutamate and small peptides. By contrast, acetylcholine, dopamine, noradrenaline, octopamine, serotonin and histamine were recruited as canonical neurotransmitters relatively later in animal evolution, only in bilaterians. Ligand-gated ion channels often preceded the establishment of novel neurotransmitter systems. Moreover, lineage-specific diversification of neurotransmitter receptors occurred in parallel within Cnidaria and several bilaterian lineages, including acoels. In summary, ancestral diversification of secretory signal molecules provides unique chemical microenvironments for behaviour-driven innovations that pave the way to complex brain functions and elementary cognition. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens'.
more »
« less
- Award ID(s):
- 1645219
- NSF-PAR ID:
- 10287473
- Date Published:
- Journal Name:
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Volume:
- 376
- Issue:
- 1821
- ISSN:
- 0962-8436
- Page Range / eLocation ID:
- 20190762
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Ctenophores are descendants of an early branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals.
Mnemiopsis is one of the important reference ctenophore species. However, little is known about its neuromuscular organization. Here, we mapped and tracked the development of the neural and muscular elements in the early hatching cydippid larvae, as well as adultMnemiopsis leidyi Mnemiopsis was very similar toPleurobrachia bachei , although inMnemiopsis the entire process occurred significantly faster. The subepithelial neural cells were observed immediately after hatching. This population consisted of a dozen of separated individual neurons with short neurites. In about 2 days, when their neurites grew significantly longer and connected to their neighbors, they began to form a canonical polygonal subepithelial network. Mesogleal neural elements prominent in all studied adult ctenophores were not detectable inMnemiopsis larvae but were clearly labeled in closely related Lobata speciesBolinopsis infundibulum . Hatched larvae also had putative mechanoreceptors with long stereocilia and approximately two dozen muscle cells. In adultMnemiopsis, the feeding lobes and auricles contained two distinct populations of neurons and neural ensembles that were not observed in other ctenophore lineages and likely represented elaborate neuronal innovations characteristic for the clade Lobata and their lifestyles. -
Biological systems have a variety of time-keeping mechanisms ranging from molecular clocks within cells to a complex interconnected unit across an entire organism. The suprachiasmatic nucleus, comprising interconnected oscillatory neurons, serves as a master-clock in mammals. The ubiquity of such systems indicates an evolutionary benefit that outweighs the cost of establishing and maintaining them, but little is known about the process of evolutionary development. To begin to address this shortfall, we introduce and analyse a new evolutionary game theoretic framework modelling the behaviour and evolution of systems of coupled oscillators. Each oscillator is characterized by a pair of dynamic behavioural dimensions, a phase and a communication strategy, along which evolution occurs. We measure success of mutations by comparing the benefit of synchronization balanced against the cost of connections between the oscillators. Despite the simple set-up, this model exhibits non-trivial behaviours mimicking several different classical games—the Prisoner’s Dilemma, snowdrift games, coordination games—as the landscape of the oscillators changes over time. Across many situations, we find a surprisingly simple characterization of synchronization through connectivity and communication: if the benefit of synchronization is greater than twice the cost, the system will evolve towards complete communication and phase synchronization.more » « less
-
more » « less
Abstract Although, neurosensory systems might have evolved independently in ctenophores, very little is known about their organization and functions. Most ctenophores are pelagic and deep‐water species and cannot be bred in the laboratory. Thus, it is not surprising that neuroanatomical data are available for only one genus within the group—
Pleurobrachia . Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of two distinct neural subsystems (subepithelial and mesogleal) and the structure of different receptor types in the comb jellyBeroe abyssicola —Beroe , with five receptor types, covers the entire body surface and expands deep into the pharynx. Three types of mesogleal neurons are comparable to the cydippidPleurobrachia . The predatory lifestyle ofBeroe is supported by the extensive development of ciliated and muscular structures including the presence of giant muscles and feeding macrocilia. The obtained cell‐type atlas illustrates different examples of lineage‐specific innovations within these enigmatic marine animals and reveals the remarkable complexity of sensory and effector systems in this clade of basal Metazoa. -
Thinking about possibilities plays a critical role in the choices humans make throughout their lives. Despite this, the influence of individuals' ability to consider what is possible on culture has been largely overlooked. We propose that the ability to reason about future possibilities or prospective cognition, has consequences for cultural change, possibly facilitating the process of cumulative cultural evolution. In particular, by considering potential future costs and benefits of specific behaviours, prospective cognition may lead to a more flexible use of cultural behaviours. In species with limited planning abilities, this may lead to the development of cultures that promote behaviours with future benefits, circumventing this limitation. Here, we examine these ideas from a comparative perspective, considering the relationship between human and nonhuman assessments of future possibilities and their cultural capacity to invent new solutions and improve them over time. Given the methodological difficulties of assessing prospective cognition across species, we focus on planning, for which we have the most data in other species. Elucidating the role of prospective cognition in culture will help us understand the variability in when and how we see culture expressed, informing ongoing debates, such as that surrounding which social learning mechanisms underlie culture. This article is part of the theme issue ‘Thinking about possibilities: mechanisms, ontogeny, functions and phylogeny’.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rstb.2019.0762
