A Distinct Contractile Injection System Found in a Majority of Adult Human Microbiomes

Rojas, María Isabel; Cavalcanti, Giselle S.; McNair, Katelyn; Benler, Sean; Alker, Amanda T.; Cobián-Güemes, Ana G; Giluso, Melissa; Levi, Kyle; Rohwer, Forest; Beyhan, Sinem; Edwards, Robert A.; Shikuma, Nicholas J.

doi:10.1101/865204

Cited by 3 publications

(4 citation statements)

References 54 publications

(74 reference statements)

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“…However, we detected a mild eCIS enrichment in the human gut commensal Bacteroides ( Figure 1B) and Parabacteroidetes genera. Bacteroides was recently reported by the Shikuma group as being eCIS-rich 28 .…”

Section: Ecis Presence Is Highly Correlated With Specific Ecosystemsmentioning

confidence: 96%

The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins

Geller

Pollin

Zlotkin

et al. 2020

Preprint

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Bacteria employ toxin delivery systems to exclude bacterial competitors and to infect host cells. Characterization of these systems and the toxins they secrete is important for understanding microbial interactions and virulence in different ecosystems. The extracellular Contractile Injection System (eCIS) is a toxin delivery particle that evolved from a bacteriophage tail. Four known eCIS systems have been shown to mediate interactions between bacteria and their invertebrate hosts, but the broad ecological function of these systems remains unknown. Here, we identify eCIS loci in 1,249 prokaryotic genomes and reveal a striking enrichment of these loci in environmental microbes and absence from mammalian pathogens. We uncovered 13 toxin genes that associate with eCIS from diverse microbes and show that they can inhibit growth of bacteria, yeast or both. We also found immunity genes that protect bacteria from self-intoxication, supporting an antibacterial role for eCIS. Furthermore, we identified multiple new eCIS core genes including a conserved eCIS transcriptional regulator. Finally, we present our data through eCIStem; an extensive eCIS repository. Our findings define eCIS as a widespread environmental prokaryotic toxin delivery system that likely mediates antagonistic interactions with eukaryotes and prokaryotes. Future understanding of eCIS functions can be leveraged for the development of new biological control systems, antimicrobials, and cell-free protein delivery tools.

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Section: Ecis Presence Is Highly Correlated With Specific Ecosystemsmentioning

confidence: 96%

The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins

Geller

Pollin

Zlotkin

et al. 2020

Preprint

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“…MACs are one example of contractile injection systems (CISs), which are related to the contractile tails of some bacteriophage [the viruses of bacteria (Figure 4c Since the discovery of MACs, related CISs have been discovered that also form multi-CIS complexes (13). In addition to stimulating metamorphosis, closely related structures were found to mediate interactions between microbes and amoebae, insects, and potentially humans (13,132,159,172). While a number of pathogenic bacteria use type VI secretion systems to inject protein toxins into target cells to cause disease (97), MACs are the first CIS to promote a beneficial microbeanimal interaction.…”

Section: A Surprisingly Different Way That Bacteria Stimulate Metamor...mentioning

confidence: 99%

“…Finally, bacteria-stimulated metamorphosis is a widespread example of a beneficial host-microbe interaction, yet it is a largely unexplored space for mining of biomedical and biotechnology applications. For example, based on our discovery of MACs, we identified a new and previously undescribed family of CISs that are produced by Bacteroidales bacteria commonly found in the human gut (132). Such systems inject contents into diverse animal cell types and could someday be modified as nanometer-scale devices for the delivery of specific proteins into target cells (130).…”

Section: Applied Potential Of Studying How Bacteria Stimulate Animal ...mentioning

confidence: 99%

The Influence of Bacteria on Animal Metamorphosis

Cavalcanti

Alker

Delherbe

et al. 2020

Annu. Rev. Microbiol.

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The swimming larvae of many marine animals identify a location on the seafloor to settle and undergo metamorphosis based on the presence of specific surface-bound bacteria. While bacteria-stimulated metamorphosis underpins processes such as the fouling of ship hulls, animal development in aquaculture, and the recruitment of new animals to coral reef ecosystems, little is known about the mechanisms governing this microbe-animal interaction. Here we review what is known and what we hope to learn about how bacteria and the factors they produce stimulate animal metamorphosis. With a few emerging model systems, including the tubeworm Hydroides elegans, corals, and the hydrozoan Hydractinia, we have begun to identify bacterial cues that stimulate animal metamorphosis and test hypotheses addressing their mechanisms of action. By understanding the mechanisms by which bacteria promote animal metamorphosis, we begin to illustrate how, and explore why, the developmental decision of metamorphosis relies on cues from environmental bacteria.

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“…The products bacteria produce to promote Hydroides metamorphosis and the machinery Hydroides uses to sense these products could lead to broader discoveries about mechanisms and tools for host-microbe interactions. For example, we found that gene clusters encoding Contractile Injection Systems originally discovered to promote Hydroides metamorphosis are strikingly similar to gene clusters found in Bacteroidales bacteria from healthy human microbiomes 62 . Moreover, understanding the payload delivery and targeting mechanism of the MACs produced by P. luteoviolacea could enable us to produce new types of therapeutic delivery systems 63 .…”

Section: Biotechnology and Bacterial Productsmentioning

confidence: 61%

Developmental staging and future research directions of the model marine tubewormHydroides elegans

Nesbit

Shikuma

2022

Preprint

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Background: The marine tube worm modelHydroides elegansis an emerging system for probing the molecular foundations of bacterial influences on development. However, a complete description of the life cycle from fertilization through sexual maturity remains scattered in the literature, and lacks standardization. Results: Here we present a unified staging scheme detailing the major morphological changes that occur during the entire life cycle of the animal. These data represent the most complete record of the entire life cycle, and serve as a foundation for connecting molecular changes with morphology. Conclusions: These descriptions and associated staging scheme are especially timely as this system gains traction within research communities. As a frontrunning animal model for studying how bacteria stimulate development, characterizing major developmental events like metamorphosis in greater resolution is essential for future investigation of the molecular mechanisms in bacteria and in the worm host that are driving these changes.

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A Distinct Contractile Injection System Found in a Majority of Adult Human Microbiomes

Abstract: 30

Cited by 3 publications

References 54 publications

The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins

The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins

The Influence of Bacteria on Animal Metamorphosis

Developmental staging and future research directions of the model marine tubewormHydroides elegans

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