Impact of simulated microgravity on the normal developmental time line of an animal-bacteria symbiosis

Foster, Jamie S.; Khodadad, Christina L.; Ahrendt, Steven; Parrish, Mirina L

doi:10.1038/srep01340

Cited by 30 publications

(61 citation statements)

References 61 publications

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“…The phagocytic capabilities of circulating neutrophils obtained from these postflight astronauts were decreased, whereas the adhesion to endothelial cells was increased (5,6). Monocytes from the blood also showed altered pro-and antiinflammatory cytokine production, increased TLR4 but decreased CD14 expressions, reduced ability to engulf pathogenic Escherichia coli, and an inability to generate an oxidative burst (4,(7)(8)(9). Altered T cell distribution and cytokine production, decreased T cell activation, proliferation, cytotoxic functions, and decreased NK functions were also observed (4,10,11).…”

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Simulated microgravity disrupts intestinal homeostasis and increases colitis susceptibility

Li¹,

Shi²,

Zhang³

et al. 2015

The FASEB Journal

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The immune systems can be altered by spaceflight in many aspects, but microgravity-related mucosal immune changes and its clinical significance have not been well studied. The purpose of this study was to investigate whether simulated microgravity influences the intestinal homeostasis and increases the susceptibility to colon inflammation. The hindlimb unloading (HU) mouse model was used to simulate the microgravity condition. Three percent dextran sulfate sodium (DSS) was given to mice to induce colitis. Compared to ground control (Ctrl) mice, the HU ones revealed an impaired intestinal homeostasis and increased susceptibility to DSS-induced colitis. This includes an early-onset, 4-fold expansion of segmented filamentous bacteria (SFB), more than 2-fold decrease in regulatory T (Treg) cell numbers and IL-10 production, ∼2-fold increase in colonic IL-1β expression, 2-fold increase in circulating neutrophils, and colonic neutrophil infiltration. The application of antibiotics ameliorated the Treg and IL-10 reductions but did not significantly dampen neutrophilia and elevated expression of colonic IL-1β. These results indicate that the intestinal microflora and innate immune system both respond to simulated microgravity and together, contribute to the proinflammatory shift in the gut microenvironment. The data also emphasize the necessity for evaluating the susceptibility to inflammatory bowel diseases (IBDs) in distant space travels.

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Simulated microgravity disrupts intestinal homeostasis and increases colitis susceptibility

Li¹,

Shi²,

Zhang³

et al. 2015

The FASEB Journal

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“…A previous study implicated that gelanolytic activity via a matrix metalloproteinase (MMP) may contribute to this process (Koropatnick et al, 2014) and other work has shown an increase in MMP expression in the light organs of colonized juveniles (Chun et al, 2008) and in hemocytes from symbiotic compared to antibiotic-treated (cured) adult hosts (Collins et al, 2012a; Schleicher et al, 2014). However, regression of the ciliated appendages may not be entirely dependent upon hemocytes, as squid colonized by V. fischeri in simulated microgravity showed a decrease in hemocyte trafficking but an accelerated restructuring of the ciliated appendages (Foster et al, 2013). …”

Section: Hemocyte Interactions With V Fischerimentioning

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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“…To examine the impact of microgravity on beneficial host-microbe interactions in situ , the symbiosis between the Hawaiian bobtail squid Euprymna scolopes and its bioluminescent partner Vibrio fischeri has emerged as tractable model for space biology research24252627. For almost 30 years, this mutualism has enabled the elucidation of fundamental principles associated with horizontally acquired symbioses and their influence on normal animal development282930.…”

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confidence: 99%

“…Under modeled microgravity conditions, however, many of these bacteria-induced developmental events are altered2627. For example, the trafficking of the hemocytes into the CEA blood sinus is delayed by 10 h in symbiotic animals, and the number of hemocytes within the sinus never reaches levels observed in gravity controls26.…”

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confidence: 99%

“…For example, the trafficking of the hemocytes into the CEA blood sinus is delayed by 10 h in symbiotic animals, and the number of hemocytes within the sinus never reaches levels observed in gravity controls26. Additionally, the onset of apoptosis and regression of the CEA structures after colonization is accelerated compared to the normal developmental timeline under simulated microgravity conditions26. Although there are clear phenotypes associated with the modeled microgravity, many of the underlying molecular changes are unknown.…”

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confidence: 99%

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Transcriptomic changes in an animal-bacterial symbiosis under modeled microgravity conditions

Casaburi

Goncharenko-Foster

Duscher

et al. 2017

Sci Rep

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Spaceflight imposes numerous adaptive challenges for terrestrial life. The reduction in gravity, or microgravity, represents a novel environment that can disrupt homeostasis of many physiological processes. Additionally, it is becoming increasingly clear that an organism’s microbiome is critical for host health and examining its resiliency in microgravity represents a new frontier for space biology research. In this study, we examine the impact of microgravity on the interactions between the squid Euprymna scolopes and its beneficial symbiont Vibrio fischeri, which form a highly specific binary mutualism. First, animals inoculated with V. fischeri aboard the space shuttle showed effective colonization of the host light organ, the site of the symbiosis, during space flight. Second, RNA-Seq analysis of squid exposed to modeled microgravity conditions exhibited extensive differential gene expression in the presence and absence of the symbiotic partner. Transcriptomic analyses revealed in the absence of the symbiont during modeled microgravity there was an enrichment of genes and pathways associated with the innate immune and oxidative stress response. The results suggest that V. fischeri may help modulate the host stress responses under modeled microgravity. This study provides a window into the adaptive responses that the host animal and its symbiont use during modeled microgravity.

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Impact of simulated microgravity on the normal developmental time line of an animal-bacteria symbiosis

Cited by 30 publications

References 61 publications

Simulated microgravity disrupts intestinal homeostasis and increases colitis susceptibility

Simulated microgravity disrupts intestinal homeostasis and increases colitis susceptibility

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

Transcriptomic changes in an animal-bacterial symbiosis under modeled microgravity conditions

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