Leisingera sp. JC1, a Bacterial Isolate from Hawaiian Bobtail Squid Eggs, Produces Indigoidine and Differentially Inhibits Vibrios

Gromek, Samantha M.; Suria, Andrea M.; Fullmer, Matthew S.; Garcia, Jillian L.; Gogarten, J. Peter; Nyholm, Spencer V.; Balunas, Marcy J.

doi:10.3389/fmicb.2016.01342

Cited by 70 publications

(81 citation statements)

References 65 publications

(113 reference statements)

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“…JC1, a member of the roseobacter clade ( Rhodobacteraceae ) of Alphaproteobacteria. 25 As is characteristic of many cephalopod species, female Hawaiian bobtail squids house a bacterial community in the accessory nidamental gland (ANG), part of their reproductive systems. Bacteria are deposited into eggs that are then laid in locations where they are vulnerable to an assortment of threats as they must develop further.…”

Section: Animal-microbe Symbiosesmentioning

confidence: 99%

“…JC1 is a critical element of the symbiont community in bobtail squid ANGs and that this bacterium houses a number of biosynthetic gene clusters (BGCs) for a number of secondary metabolites, including siderophores and quorum-associated acyl-homoserine lactones. 25 Leisingera sp. JC1 was found to produce the pigment indigoidine both, in isolation, and in co-culture conditions with Vibrio fischeri , the light organ bacterial symbiont of E. scolopes , as well as with other Vibrio spp.…”

Section: Animal-microbe Symbiosesmentioning

confidence: 99%

“…Auto-regulation of biosynthesis is coordinated through QS molecules including acyl-homoserine lactones and γ-butyrolactones in Gram-negative and Gram-positive bacteria, respectively. These systems, which serve ecological functions as described in the aforementioned symbiosis between Hawaiiain bobtail squid and bacteria, 25 have been utilized in the laboratory to induce antibiotic production. A rigorous survey detailing the regulation of antibiotic biosyntheses through interspecies interactions, including QS-mediated interactions, has recently appeared.…”

Section: Antibiotic Discovery Guided By Microbial Interactionsmentioning

confidence: 99%

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Symbiosis-inspired approaches to antibiotic discovery

2017

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Life on Earth is characterized by a remarkable abundance of symbiotic and highly refined relationships among life forms. Defined as any kind of close, long-term association between two organisms, symbioses can be mutualistic, commensalistic or parasitic. Historically speaking, selective pressures have shaped symbioses in which one organism (typically a bacterium or fungus) generates bioactive small molecules that impact the host (and possibly other symbionts); the symbiosis is driven fundamentally by the genetic machineries available to the small molecule producer. The human microbiome is now integral to the most recent chapter in animal-microbe symbiosis studies and plant-microbe symbioses have significantly advanced our understanding of natural products biosynthesis; this also is the case for studies of fungal-microbe symbioses. However, much less is known about microbe-microbe systems involving interspecies interactions. Microbe-derived small molecules (i.e. antibiotics and quorum sensing molecules, etc.) have been shown to regulate transcription in microbes within the same environmental niche, suggesting interspecies interactions whereas, intraspecies interactions, such as those that exploit autoinducing small molecules, also modulate gene expression based on environmental cues. We, and others, contend that symbioses provide almost unlimited opportunities for the discovery of new bioactive compounds whose activities and applications have been evolutionarily optimized. Particularly intriguing is the possibility that environmental effectors can guide laboratory expression of secondary metabolites from “orphan”, or silent, biosynthetic gene clusters (BGCs). Notably, many of the studies summarized here result from advances in “omics” technologies and highlight how symbioses have given rise to new anti-bacterial and antifungal natural products now being discovered.

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Section: Animal-microbe Symbiosesmentioning

confidence: 99%

Section: Animal-microbe Symbiosesmentioning

confidence: 99%

Section: Antibiotic Discovery Guided By Microbial Interactionsmentioning

confidence: 99%

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Symbiosis-inspired approaches to antibiotic discovery

2017

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“…This gland is composed of many epithelium-lined tubules, containing a bacterial consortium dominated by members of the Alphaproteobacteria and Verrucomicrobia (Collins et al, 2012b). The bacteria are deposited into the egg jelly coats of squid where they are hypothesized to play a protective role during development (Collins et al, 2012b, 2015; Gromek et al, 2016). Like the light organ, the ANG is highly vascularized and hemocytes have been observed within the lumen of the tubules and in direct contact with bacteria ( Figure 1C ; Collins et al, 2012b).…”

Section: E Scolopes As a Model For Binary And Consortial Symbiosesmentioning

confidence: 99%

“…Studies in a number of animal-microbe symbioses have revealed that bacteria are active in a wide range of biological processes (McFall-Ngai et al, 2013), including digestion, host defense, development, and even camouflage (Gil-Turnes et al, 1989; McFall-Ngai and Montgomery, 1990; Jones and Nishiguchi, 2004; Kau et al, 2011; Hooper et al, 2012; Fraune et al, 2015; Gromek et al, 2016). Interactions between hosts’ immune systems and the resident microbiota are often essential in the establishment and maintenance of beneficial associations (Stappenbeck et al, 2002; Nyholm and Graf, 2012; Buchon et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host–Microbe Interactions

McAnulty

Nyholm

2017

Front. Microbiol.

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Most, if not all, animals engage in associations with bacterial symbionts. Understanding the mechanisms by which host immune systems and beneficial bacteria communicate is a fundamental question in the fields of immunology and symbiosis. The Hawaiian bobtail squid (Euprymna scolopes) engages in two known symbioses; a binary relationship with the light organ symbiont Vibrio fischeri, and a bacterial consortium within a specialized organ of the female reproductive system, the accessory nidamental gland (ANG). E. scolopes has a well-developed circulatory system that allows immune cells (hemocytes) to migrate into tissues, including the light organ and ANG. In the association with V. fischeri, hemocytes are thought to have a number of roles in the management of symbiosis, including the recognition of non-symbiotic bacteria and the contribution of chitin as a nutrient source for V. fischeri. Hemocytes are hypothesized to recognize bacteria through interactions between pattern recognition receptors and microbe-associated molecular patterns. Colonization by V. fischeri has been shown to affect the bacteria-binding behavior, gene expression, and proteome of hemocytes, indicating that the symbiont can modulate host immune function. In the ANG, hemocytes have also been observed interacting with the residing bacterial community. As a model host, E. scolopes offers a unique opportunity to study how the innate immune system interacts with both a binary and consortial symbiosis. This mini review will recapitulate what is known about the role of hemocytes in the light organ association and offer future directions for understanding how these immune cells interact with multiple types of symbioses.

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