Regulation of axial and head patterning during planarian regeneration by a commensal bacterium

Williams, Katherine B.; Bischof, Johanna; Lee, Frederick J.; Miller, Kelsie A.; LaPalme, Jennifer V.; Wolfe, Benjamin E.; Levin, Michael

doi:10.1016/j.mod.2020.103614

Cited by 23 publications

(21 citation statements)

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“…First are the neighboring agents, such as other tissues, which pass on their bioelectric state during cooperative and competitive interactions in morphogenesis. There are also commensal and parasitic microbes, which have evolved to hijack such control systems to manipulate the anatomy of the host—like the naïve bacteria on planaria that can determine head number and visual system structure in flatworm regeneration ( Williams et al, 2020 ). Moreover, the development of pharmacological, genetic, and optogenetic tools now allows human bioengineers to access bioelectrical circuits for the control of growth and form in regenerative medicine and synthetic bioengineering contexts ( Adams et al, 2013 , 2014 , 2016 ; Chernet et al, 2016 ; McNamara et al, 2016 ; Bonzanni et al, 2020 ).…”

Section: Evolutionary Aspectsmentioning

confidence: 99%

Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds

Levin

2022

Front. Syst. Neurosci.

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135

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Synthetic biology and bioengineering provide the opportunity to create novel embodied cognitive systems (otherwise known as minds) in a very wide variety of chimeric architectures combining evolved and designed material and software. These advances are disrupting familiar concepts in the philosophy of mind, and require new ways of thinking about and comparing truly diverse intelligences, whose composition and origin are not like any of the available natural model species. In this Perspective, I introduce TAME—Technological Approach to Mind Everywhere—a framework for understanding and manipulating cognition in unconventional substrates. TAME formalizes a non-binary (continuous), empirically-based approach to strongly embodied agency. TAME provides a natural way to think about animal sentience as an instance of collective intelligence of cell groups, arising from dynamics that manifest in similar ways in numerous other substrates. When applied to regenerating/developmental systems, TAME suggests a perspective on morphogenesis as an example of basal cognition. The deep symmetry between problem-solving in anatomical, physiological, transcriptional, and 3D (traditional behavioral) spaces drives specific hypotheses by which cognitive capacities can increase during evolution. An important medium exploited by evolution for joining active subunits into greater agents is developmental bioelectricity, implemented by pre-neural use of ion channels and gap junctions to scale up cell-level feedback loops into anatomical homeostasis. This architecture of multi-scale competency of biological systems has important implications for plasticity of bodies and minds, greatly potentiating evolvability. Considering classical and recent data from the perspectives of computational science, evolutionary biology, and basal cognition, reveals a rich research program with many implications for cognitive science, evolutionary biology, regenerative medicine, and artificial intelligence.

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Section: Evolutionary Aspectsmentioning

confidence: 99%

Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds

Levin

2022

Front. Syst. Neurosci.

Self Cite

135

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show abstract

“…First are the neighboring agents, such as other tissues, which pass on their bioelectric state during cooperative and competitive interactions in morphogenesis. There are also commensal and parasitic microbes, which have evolved was to hijack such control systems to manipulate the anatomy of the host -like the naïve bacteria on planaria that can determine head number and visual system structure in flatworm regeneration [272]. Moreover, the development of pharmacological, genetic, and optogenetic tools now allows human bioengineers to access bioelectrical circuits for the control of growth and form in regenerative medicine and synthetic bioengineering contexts [273; 274; 275; 276; 277; 278].…”

Section: Somatic Bioelectrics Reveals the Origin Of Complex Cognitive Systemsmentioning

confidence: 99%

Technological Approach to Mind Everywhere (TAME): an experimentally- grounded framework for understanding diverse bodies and minds

Levin¹

2021

Preprint

Self Cite

View full text Add to dashboard Cite

Synthetic biology and bioengineering provide the opportunity to create novel embodied cognitive systems (otherwise known as minds) in a very wide variety of chimeric architectures combining evolved and designed material and software. These advances are disrupting familiar concepts in the philosophy of mind, and require new ways of thinking about and comparing truly diverse intelligences, whose composition and origin are not like any of the available natural model species. In this Perspective, I introduce TAME - Technological Approach to Mind Everywhere - a framework for understanding and manipulating cognition in unconventional substrates. TAME formalizes a non-binary (continuous), empirically-based approach to strongly embodied agency. When applied to regenerating/developmental systems, TAME suggests a perspective on morphogenesis as an example of basal cognition. The deep symmetry between problem-solving in anatomical, physiological, transcriptional, and 3D (traditional behavioral) spaces drives specific hypotheses by which cognitive capacities can scale during evolution. An important medium exploited by evolution for joining active subunits into greater agents is developmental bioelectricity, implemented by pre-neural use of ion channels and gap junctions to scale cell-level feedback loops into anatomical homeostasis. This architecture of multi-scale competency of biological systems has important implications for plasticity of bodies and minds, greatly potentiating evolvability. Considering classical and recent data from the perspectives of computational science, evolutionary biology, and basal cognition, reveals a rich research program with many implications for cognitive science, evolutionary biology, regenerative medicine, and artificial intelligence.

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“…Aquitalea sp . FJL05, a gram-negative commensal bacterium of another planarian, Dugesia japonica , can dramatically affect the pattern of regeneration, resulting in worms with two heads (Williams et al 2020). In this case however, indole, a small molecule produced by Aquitalia , rather than LPS, was the cause of the effect.…”

Section: Discussionmentioning

confidence: 99%

“…Raising tadpoles the presence of aminoglycoside antibiotics, which is often done prophylactically in labs and would be expected to alter the microbiome, reduces the percentage of regenerators in a cohort (Bishop and Beck 2021), suggesting that the microbiome may be important in refractory period regeneration efficiency. Microbiomes are important for wound healing in a lot of model animal systems, including planarians (Arnold et al 2016; Williams et al 2020) and mice (Velasco et al 2021; Wang et al 2021). Among these examples, indole (an aromatic amino acid metabolite produced by gut bacteria) (Williams et al 2020) and the inflammatory cytokine IL-1β (Wang et al 2021) have been implicated as critical components of the signalling pathway leading to regeneration.…”

Section: Introductionmentioning

confidence: 99%

“…Microbiomes are important for wound healing in a lot of model animal systems, including planarians (Arnold et al 2016; Williams et al 2020) and mice (Velasco et al 2021; Wang et al 2021). Among these examples, indole (an aromatic amino acid metabolite produced by gut bacteria) (Williams et al 2020) and the inflammatory cytokine IL-1β (Wang et al 2021) have been implicated as critical components of the signalling pathway leading to regeneration.…”

Section: Introductionmentioning

confidence: 99%

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Manipulating the microbiome alters regenerative outcomes inXenopus laevistadpoles via lipopolysaccharide signalling

Chapman

Gilbert

Devine

et al. 2021

Preprint

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Xenopus laevis tadpoles can regenerate functional tails, containing spinal cord, notochord, muscle, fin, blood vessels and nerves, except for a brief refractory period at around one week of age. At this stage, amputation of the tadpole's tail may either result in scarless wound healing, or the activation of a regeneration programme, which replaces the lost tissues. We recently demonstrated a link between bacterial lipopolysaccharides and successful tail regeneration in refractory stage tadpoles, and proposed that this could result from lipopolysaccharides binding to Toll-like receptor 4 (TLR4). Here, we have used 16S rRNA sequencing to show that the tadpole skin microbiome is highly variable between sibships and that the community can be altered by raising embryos in the antibiotic gentamicin. Six gram-negative genera, including Delftia and Chryseobacterium, were over-represented in tadpoles that underwent tail regeneration. Lipopolysaccharides purified from a commensal Chryseobacterium spp. XDS4, an exogenous Delftia spp. or Escherichia coli could significantly increase the number of antibiotic-raised tadpoles that attempted regeneration. Conversely, the quality of regeneration was impaired in native-raised tadpoles exposed to the antagonistic lipopolysaccharide of Rhodobacter sphaeroides. Knocking down TLR4 using CRISPR/Cas9 also reduced regeneration quality, but not quantity, at the level of the cohort. However, we found that the editing level of individual tadpoles was a poor predictor of regenerative outcome. In conclusion, our results suggest that variable regeneration in refractory stage tadpoles depends at least in part on the skin microbiome and lipopolysaccharide signalling, but that signalling via TLR4 cannot account for all of this effect.

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Regulation of axial and head patterning during planarian regeneration by a commensal bacterium

Cited by 23 publications

References 124 publications

Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds

Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds

Technological Approach to Mind Everywhere (TAME): an experimentally- grounded framework for understanding diverse bodies and minds

Manipulating the microbiome alters regenerative outcomes inXenopus laevistadpoles via lipopolysaccharide signalling

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