Cross-Kingdom Chemical Communication Drives a Heritable, Mutually Beneficial Prion-Based Transformation of Metabolism

Jarosz, Daniel F.; Brown, Jessica C. S.; Walker, Gordon A.; Datta, Manoshi Sen; Ung, W. Lloyd; Lancaster, Alex K.; Rotem, Assaf; Chang, Anna; Newby, Gregory A.; Weitz, David A.; Bisson, Linda F.; Lindquist, Susan

doi:10.1016/j.cell.2014.07.025

Cited by 151 publications

(159 citation statements)

References 51 publications

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“…Also, instead of high-molecular-weight amyloids, LDPrD-GFP formed low-molecular-weight oligomers. We have previously shown that at least one fungal prion, [GAR+], does not form amyloid or require Hsp104; instead, this prion is Hsp70-dependent (36,37). Therefore, it is possible that [LD+] belongs to this noncanonical class of prions.…”

Section: Discussionmentioning

confidence: 99%

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Luminidependens (LD) is an Arabidopsis protein with prion behavior

Chakrabortee

Kayatekin

Newby

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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171

141

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Prion proteins provide a unique mode of biochemical memory through self-perpetuating changes in protein conformation and function. They have been studied in fungi and mammals, but not yet identified in plants. Using a computational model, we identified candidate prion domains (PrDs) in nearly 500 plant proteins. Plant flowering is of particular interest with respect to biological memory, because its regulation involves remembering and integrating previously experienced environmental conditions. We investigated the prion-forming capacity of three prion candidates involved in flowering using a yeast model, where prion attributes are well defined and readily tested. In yeast, prions heritably change protein functions by templating monomers into higherorder assemblies. For most yeast prions, the capacity to convert into a prion resides in a distinct prion domain. Thus, new prionforming domains can be identified by functional complementation of a known prion domain. The prion-like domains (PrDs) of all three of the tested proteins formed higher-order oligomers. Uniquely, the Luminidependens PrD (LDPrD) fully replaced the prion-domain functions of a well-characterized yeast prion, Sup35. Our results suggest that prion-like conformational switches are evolutionarily conserved and might function in a wide variety of normal biological processes.prions | Luminidependens | plant prion domains

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Section: Discussionmentioning

confidence: 99%

“…S3 A-C). Although most known yeast prions are dependent on Hsp104, recently emerging evidence indicates that other molecular chaperones like Hsp70 and, potentially, Hsp90 may play Hsp104-independent roles in prion biology (9,36,37 (Fig. 4A).…”

Section: Identification and Functional Classification Of Arabidopsis mentioning

confidence: 99%

Luminidependens (LD) is an Arabidopsis protein with prion behavior

Chakrabortee

Kayatekin

Newby

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

171

141

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“…Waddington stressed the importance of cytoplasmic compounds and their effect on gene expression (Waddington 1935), yet maternal or transgenerational effects mediated by cytoplasmic transfer from mother to offspring would not be considered epigenetic under Holliday's definition because the expression pattern of the offspring is not independent and simply results from the transfer of cytoplasmic compounds, such as RNA, transcription factors, prions, etc. (Ptashne 2008;Jarosz et al 2014). These issues make the contrast between Waddington's epigenetics and Holliday's epigenetics much more evident.…”

Section: Heritabilitymentioning

confidence: 99%

What Do You Mean, “Epigenetic”?

2015

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Interest in the field of epigenetics has increased rapidly over the last decade, with the term becoming more identifiable in biomedical research, scientific fields outside of the molecular sciences, such as ecology and physiology, and even mainstream culture. It has become increasingly clear, however, that different investigators ascribe different definitions to the term. Some employ epigenetics to explain changes in gene expression, others use it to refer to transgenerational effects and/or inherited expression states. This disagreement on a clear definition has made communication difficult, synthesis of epigenetic research across fields nearly impossible, and has in many ways biased methodologies and interpretations. This article discusses the history behind the multitude of definitions that have been employed since the conception of epigenetics, analyzes the components of these definitions, and offers solutions for clarifying the field and mitigating the problems that have arisen due to these definitional ambiguities.

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“…One important goal within these efforts is to understand how microbes interact with each other and the consequences of such interactions at the level of their transcriptomes, proteomes, and metabolomes. For instance, it has been demonstrated that the metabolism of yeast can be transformed by bacteria-induced prions to decrease the release of inhibiting ethanol (7). In another study, an oral biofilm of the genus Streptococcus displayed different transcriptional responses toward the presence of other species in mixed-species cultures (8).…”

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confidence: 99%

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

Krause

Johnson

Karunaratne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

144

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The utilization of methane, a potent greenhouse gas, is an important component of local and global carbon cycles that is characterized by tight linkages between methane-utilizing (methanotrophic) and nonmethanotrophic bacteria. It has been suggested that the methanotroph sustains these nonmethanotrophs by cross-feeding, because subsequent products of the methane oxidation pathway, such as methanol, represent alternative carbon sources. We established cocultures in a microcosm model system to determine the mechanism and substrate that underlay the observed cross-feeding in the environment. Lanthanum, a rare earth element, was applied because of its increasing importance in methylotrophy. We used co-occurring strains isolated from Lake Washington sediment that are involved in methane utilization: a methanotroph and two nonmethanotrophic methylotrophs. Gene-expression profiles and mutant analyses suggest that methanol is the dominant carbon and energy source the methanotroph provides to support growth of the nonmethanotrophs. However, in the presence of the nonmethanotroph, gene expression of the dominant methanol dehydrogenase (MDH) shifts from the lanthanide-dependent MDH (XoxF)-type, to the calcium-dependent MDH (MxaF)-type. Correspondingly, methanol is released into the medium only when the methanotroph expresses the MxaF-type MDH. These results suggest a cross-feeding mechanism in which the nonmethanotrophic partner induces a change in expression of methanotroph MDHs, resulting in release of methanol for its growth. This partner-induced change in gene expression that benefits the partner is a paradigm for microbial interactions that cannot be observed in studies of pure cultures, underscoring the importance of synthetic microbial community approaches to understand environmental microbiomes. M icrobial communities and their members are part of every ecosystem and drive important biogeochemical processes on Earth (1). They typically comprise a range of phylogenetically and functionally diverse microbes (2) that are structured by biotic and abiotic factors (3) and are entangled through specific interactions in complex networks (4).The significance of microbial communities in diverse ecosystems including the human body is now widely accepted in science and has led to a range of initiatives focused on the world's microbiomes (5, 6). One important goal within these efforts is to understand how microbes interact with each other and the consequences of such interactions at the level of their transcriptomes, proteomes, and metabolomes. For instance, it has been demonstrated that the metabolism of yeast can be transformed by bacteria-induced prions to decrease the release of inhibiting ethanol (7). In another study, an oral biofilm of the genus Streptococcus displayed different transcriptional responses toward the presence of other species in mixed-species cultures (8).Measuring interactions in complex environmental communities is still a difficult task. Laboratory cocultures represent a simplified approach to assessing...

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Cross-Kingdom Chemical Communication Drives a Heritable, Mutually Beneficial Prion-Based Transformation of Metabolism

Cited by 151 publications

References 51 publications

Luminidependens (LD) is an Arabidopsis protein with prion behavior

Luminidependens (LD) is an Arabidopsis protein with prion behavior

What Do You Mean, “Epigenetic”?

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

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