Lessons from simple marine models on the bacterial regulation of eukaryotic development

Woznica, Arielle; King, Nicole

doi:10.1016/j.mib.2017.12.013

Cited by 37 publications

(39 citation statements)

References 52 publications

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“…There is a growing interest in the role of metabolites as chemical mediators in cross-kingdom interactions within aquatic systems (22). Molecular cues from environmental bacteria can influence the growth, development, and morphogenesis of the eukaryotes (23). The importance of bacterial biofilms in inducing larval settlement and metamorphosis of marine invertebrates has been described, but few molecular cues produced by bacteria have been identified.…”

Section: Discussionmentioning

confidence: 99%

“…Consistently, our study found that four of six inducing strains were gammaproteobacteria, suggesting that gammaproteobacteria are important inducers of larval settlement and metamorphosis for M. sallei. Because colonizable surfaces in the ocean are often very limited, cues from biofilm bacteria growing on these surfaces might indicate to animals that there is a surface on which to settle (23). Furthermore, the presence of biofilms on surfaces indicates that the environment of the surfaces is suitable for the survival of organisms.…”

Section: Discussionmentioning

confidence: 99%

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Bacterial Nucleobases Synergistically Induce Larval Settlement and Metamorphosis in the Invasive Mussel Mytilopsis sallei

Dai

et al. 2019

Appl Environ Microbiol

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Marine bacterial biofilms have long been recognized as potential inducers of larval settlement and metamorphosis in marine invertebrates, but few chemical cues from bacteria have been identified. Here, we show that larval settlement and metamorphosis of an invasive fouling mussel,Mytilopsis sallei, could be induced by biofilms of bacteria isolated from its adult shells and other substrates from the natural environment. One of the strains isolated,Vibrio owensiiMS-9, showed strong inducing activity which was attributed to the release of a mixture of nucleobases including uracil, thymine, xanthine, hypoxanthine, and guanine into seawater. In particular, the synergistic effect of hypoxanthine and guanine was sufficient for the inducing activity ofV. owensiiMS-9. The presence of two or three other nucleobases could enhance, to some extent, the activity of the mixture of hypoxanthine and guanine. Furthermore, we determined that bacteria producing higher concentrations of nucleobases were more likely to induce larval settlement and metamorphosis ofM. salleithan were bacteria producing lower concentrations of nucleobases. The present study demonstrates that bacterial nucleobases play an important role in larval settlement and metamorphosis of marine invertebrates. This provides new insights into our understanding of the role of environmental bacteria in the colonization and aggregation of invasive fouling organisms and of the metabolites used as chemical mediators in cross-kingdom communication within aquatic systems.IMPORTANCEInvasive species are an increasingly serious problem globally. In aquatic ecosystems, invasive dreissenid mussels are well-known ecological and economic pests because they appear to effortlessly invade new environments and foul submerged structures with high-density aggregations. To efficiently control exotic mussel recruitment and colonization, the need to investigate the mechanisms of substrate selection for larval settlement and metamorphosis is apparent. Our work is one of very few to experimentally demonstrate that compounds produced by environmental bacteria play an important role in larval settlement and metamorphosis in marine invertebrates. Additionally, this study demonstrates that bacterial nucleobases can be used as chemical mediators in cross-kingdom communication within aquatic systems, which will enhance our understanding of how microbes induce larval settlement and metamorphosis of dreissenid mussels, and it furthermore may allow the development of new methods for application in antifouling.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Bacterial Nucleobases Synergistically Induce Larval Settlement and Metamorphosis in the Invasive Mussel Mytilopsis sallei

Dai

et al. 2019

Appl Environ Microbiol

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“…Symbiotic microbes are still important agents in the life cycles of many organisms (Woznica & King, ). In addition to their being critical during normal embryonic development, symbiotic microbes help numerous organisms to mediate metamorphosis (Freckelton et al, ; Shikuma, Antoshechkin, Medeiros, Pilhofer, & Newman, ; Smith & Rajan, ).…”

Section: The Origin Of Multicellular Life Cyclesmentioning

confidence: 99%

Evolutionary transitions revisited: Holobiont evo‐devo

Gilbert

2019

J Exp Zool Pt B

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John T. Bonner lists four essential transformations in the evolution of life: the emergence of the eukaryotic cell, meiosis, multicellularity, and the nervous system. This paper analyses the mechanisms for those transitions in light of three of Dr. Bonner's earlier hypotheses: (a) that the organism is its life cycle, (b) that evolution consists of alterations of the life cycle, and (c) that development extends beyond the body and into interactions with other organisms. Using the notion of the holobiont life cycle, this paper attempts to show that these evolutionary transitions can be accomplished through various means of symbiosis. Perceiving the organism both as an interspecies consortium and as a life cycle supports a twofold redefinition of the organism as a holobiont constructed by integrating together the life cycles of several species. These findings highlight the importance of symbiosis and the holobiont development in analyses of evolution.

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“…Eukaryotes, including animals and their closest living relatives, choanoflagellates, encounter abundant and diverse bacteria in the environment (1)(2)(3). However, interactions among eukaryotes and bacteria can be challenging to study in animal models due to the complex physiology of the hosts and the large number of oftentimes unculturable bacteria present, each of which releases diverse molecules (4)(5)(6).…”

Section: Introductionmentioning

confidence: 99%

“…1A; (14,15)). In addition, like many animals (2,16,17), S. rosetta undergoes important life history transitions in response to distinct bacterial cues. For example, a secreted (Fig.…”

Section: Introductionmentioning

confidence: 99%

Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate

Ireland

Woznica

King

2020

Appl Environ Microbiol

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Bacteria regulate the life histories of diverse eukaryotes, but relatively little is known about how eukaryotes interpret and respond to multiple bacterial cues encountered simultaneously. To explore how a eukaryote might respond to a combination of bioactive molecules from multiple bacteria, we treated the choanoflagellate Salpingoeca rosetta with two sets of bacterial cues, one that induces mating and another that induces multicellular development. We found that simultaneous exposure to both sets of cues enhanced multicellular development in S. rosetta, eliciting both larger multicellular colonies and an increase in the number of colonies. Thus, rather than conveying conflicting sets of information, these distinct bacterial cues synergize to augment multicellular development. This study demonstrates how a eukaryote can integrate and modulate its response to cues from diverse bacteria, underscoring the potential impact of complex microbial communities on eukaryotic life histories. IMPORTANCE Eukaryotic biology is profoundly influenced by interactions with diverse environmental and host-associated bacteria. However, it is not well understood how eukaryotes interpret multiple bacterial cues encountered simultaneously. This question has been challenging to address because of the complexity of many eukaryotic model systems and their associated bacterial communities. Here, we studied a close relative of animals, the choanoflagellate Salpingoeca rosetta, to explore how eukaryotes respond to diverse bacterial cues. We found that a bacterial chondroitinase that induces mating on its own can also synergize with bacterial lipids that induce multicellular “rosette” development. When encountered together, these cues enhance rosette development, resulting in both the formation of larger rosettes and an increase in the number of rosettes compared to rosette development in the absence of the chondroitinase. These findings highlight how synergistic interactions among bacterial cues can influence the biology of eukaryotes.

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Lessons from simple marine models on the bacterial regulation of eukaryotic development

Cited by 37 publications

References 52 publications

Bacterial Nucleobases Synergistically Induce Larval Settlement and Metamorphosis in the Invasive Mussel Mytilopsis sallei

Bacterial Nucleobases Synergistically Induce Larval Settlement and Metamorphosis in the Invasive Mussel Mytilopsis sallei

Evolutionary transitions revisited: Holobiont evo‐devo

Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate

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