Microbiota and the social brain

Sherwin, Eoin; Bordenstein, Seth R.; Quinn, John L.; Dinan, Timothy G.; Cryan, John F.

doi:10.1126/science.aar2016

Cited by 365 publications

(330 citation statements)

References 149 publications

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“…Our findings are also relevant beyond bees. We have identified a potential feedback 365 between host behavior and the microbiome, a topic that has recently garnered substantial interest 366 [86,87]. Specifically, we suggest that social bee thermoregulatory behaviors have provided their symbionts' thermal niches.…”

mentioning

confidence: 94%

Thermal niches of specialized gut symbionts: the case of social bees

Hammer

Moran

2020

Preprint

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1 2 Responses to climate change are particularly complicated in species that engage in 3 symbioses, as the niche of one partner may be modified by that of the other. We explored 4 thermal traits in gut symbionts of honeybees and bumblebees, which are vulnerable to rising 5 temperatures. In vitro assays of symbiont strains isolated from 16 host species revealed variation 6 in thermal niches. Strains from bumblebees tended to be less heat-tolerant than those from 7 honeybees, possibly due to bumblebees maintaining cooler nests or inhabiting cooler climates. 8Overall however, bee symbionts grew at temperatures up to 44 °C and withstood temperatures up 9 to 52 °C, at or above the upper thermal limits of their hosts. While heat-tolerant, most strains of 10 the symbiont Snodgrassella grew relatively slowly below 35 °C, perhaps because of adaptation 11 to the elevated body temperatures that bees maintain through thermoregulation. In a gnotobiotic 12 bumblebee experiment, Snodgrassella was unable to consistently colonize bees reared below 35 13 °C under conditions that limit thermoregulation. Thus, host thermoregulatory behavior appears 14 important in creating a warm microenvironment for symbiont establishment. Bee-microbiome-15 temperature interactions could affect host health and pollination services, and inform research on 16 the thermal biology of other specialized gut symbionts, such as those of humans. 17 18 19 20 Earth's climate is rapidly warming, and there is an urgent need to understand how 21 organisms will respond [1,2]. One factor complicating such predictions is the role of interspecific 22 interactions [3,4], and, in particular, symbiosis [5,6]. Many organisms closely associate with one 23 or more distantly related partners that have highly distinct physiologies, as in the case of animal 24 or plant hosts and their microbiomes. Hosts and microbes are likely to have different responses 25 to temperature; yet, if they are mutually dependent, the combined niche is restricted to that of the 26 more sensitive partner. Furthermore, thermal niches can themselves evolve in response to 27 symbiotic lifestyles. For example, obligate endosymbionts that undergo strong population 28 bottlenecks during transmission may evolve unstable, easily denatured proteins as a consequence 29 of mutation accumulation, leading to heat sensitivity [7][8][9]. Both of these factors may constrain 30 the combined thermal niche of strongly symbiont-dependent organisms [6,10,11]. There is 31 evidence for symbiont-imposed constraints on host thermotolerance in a variety of invertebrates 32 such as aphids, ants, stinkbugs, corals, and sponges [12][13][14][15][16]. However, the wider prevalence of 33 this phenomenon is unclear, and, in general, we do not know how microbiomes will influence 34 host responses to climate warming. 35The eusocial corbiculate bees (hereafter "social bees") are a particularly important group 36 in which to study symbiont thermal niches and their effects on hosts. This clade, comprising 37 honey bees (Apis), bumb...

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confidence: 94%

Thermal niches of specialized gut symbionts: the case of social bees

Hammer

Moran

2020

Preprint

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“…For example, the human colon microbiota is constituted by 100 to 300 different bacterial taxa together with dozens of fungi, archaea and viruses (Hillman et al, 2017). Also, different protists, bacteria, archaea, and viruses live in association with corals (Thompson et al, 2015;Bourne et al, 2016), whereas the bacteria covering the cuticle of two Neotropical ants belong to at least ten different phyla (Birer et al, 2017) Besides the importance of microbes in hosts' physical and mental health and even in their social behavior (Cho and Blaser, 2012;Mattoso et al, 2012;Valdes et al, 2018;Taylor, 2019;Sherwin et al, 2019), species rich soil microbiota are essential for maintaining the functioning of terrestrial ecosystems. They are involved in decomposing organic materials and in maintaining biogeochemical cycles of nitrogen and carbon (Bardgett et al, 2008;Jacoby et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Density-dependent private benefit leads to bacterial mutualism

Jimenez¹,

Scheuring

2020

Preprint

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Microorganisms produce materials leaked from the cell which are beneficial for themselves and their neighbors. We modeled the situation when cells can produce different costly secretions which increase the carrying capacity of the population. Strains that lose the function of producing one or more secretions avoid the cost of production and can exhaust the producers. However, secreting substances provides a private benefit for the producers in a density-dependent way. We developed a model to examine the outcome of the selection among different type of producer strains from the non-producer strain to the partial producers, to the full producer one. We were particularly interested in circumstances under which selection maintains partners that produce complementary secreted materials thus forming an interdependent mutualistic interaction.We show that interdependent mutualism is selected under broad range of conditions if private benefit decreases with density. Selection frequently causes the coexistence of more and less generalist cooperative strains, thus cooperation and exploitation co-occur. Interdependent mutual-ism is evolved under more specific circumstances if private benefit increases with density and these general observations are valid in a well-mixed and in a structured deme model. We show that the applied population structure supports cooperation in general, which, depending on the level of private benefit and intensity of mixing helps either the specialist or the generalist cooperators.

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“…Animalssocial behavior and cognition. Perhaps the strongest evidence for microbial modulation of cognition and behavior in animal models comes from studies of social interactions (Sherwin et al, 2019). Germ-free rodents typically exhibit deficits in both sociability and memory for social stimuli (indexed by preference for a novel social partner; Buffington et al, 2016;Desbonnet et al, 2014;Sgritta et al, 2019;Stilling et al, 2018; but see also Arentsen et al, 2015).…”

Section: Behavioral and Cognitive Developmentmentioning

confidence: 99%

Annual Research Review: Critical windows – the microbiota–gut–brain axis in neurocognitive development

Cowan

Dinan

Cryan

2019

Child Psychology Psychiatry

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128

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The gut microbiota is a vast, complex, and fascinating ecosystem of microorganisms that resides in the human gastrointestinal tract. As an integral part of the microbiota–gut–brain axis, it is now being recognized that the microbiota is a modulator of brain and behavior, across species. Intriguingly, periods of change in the microbiota coincide with the development of other body systems and particularly the brain. We hypothesize that these times of parallel development are biologically relevant, corresponding to ‘sensitive periods’ or ‘critical windows’ in the development of the microbiota–gut–brain axis. Specifically, signals from the microbiota during these periods are hypothesized to be crucial for establishing appropriate communication along the axis throughout the life span. In other words, the microbiota is hypothesized to act like an expected input to calibrate the development of the microbiota–gut–brain axis. The absence or disruption of the microbiota during specific developmental windows would therefore be expected to have a disproportionate effect on specific functions or potentially for regulation of the system as a whole. Evidence for microbial modulation of neurocognitive development and neurodevelopmental risk is discussed in light of this hypothesis, finishing with a focus on the challenges that lay ahead for the future study of the microbiota–gut–brain axis during development.

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Microbiota and the social brain

Cited by 365 publications

References 149 publications

Thermal niches of specialized gut symbionts: the case of social bees

Thermal niches of specialized gut symbionts: the case of social bees

Density-dependent private benefit leads to bacterial mutualism

Annual Research Review: Critical windows – the microbiota–gut–brain axis in neurocognitive development

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