ABSTRACT Microbes live in complex microniches within host tissues, but how symbiotic partners communicate to create such niches during development remains largely unexplored. Using confocal microscopy and symbiont genetics, we characterized the shaping of host microenvironments during light organ colonization of the squid Euprymna scolopes by the bacterium Vibrio fischeri . During embryogenesis, three pairs of invaginations form sequentially on the organ’s surface, producing pores that lead to interior compressed tubules at different stages of development. After hatching, these areas expand, allowing V. fischeri cells to enter and migrate ∼120 μm through three anatomically distinct regions before reaching blind-ended crypt spaces. A dynamic gatekeeper, or bottleneck, connects these crypts with the migration path. Once V. fischeri cells have entered the crypts, the bottlenecks narrow, and colonization by the symbiont population becomes spatially restricted. The actual timing of constriction and restriction varies with crypt maturity and with different V. fischeri strains. Subsequently, starting with the first dawn following colonization, the bottleneck controls a lifelong cycle of dawn-triggered expulsions of most of the symbionts into the environment and a subsequent regrowth in the crypts. Unlike other developmental phenotypes, bottleneck constriction is not induced by known microbe-associated molecular patterns (MAMPs) or by V. fischerimore »
The cytokine MIF controls daily rhythms of symbiont nutrition in an animal–bacterial association
The recent recognition that many symbioses exhibit daily rhythms has encouraged research into the partner dialogue that drives these biological oscillations. Here we characterized the pivotal role of the versatile cytokine macrophage migration inhibitory factor (MIF) in regulating a metabolic rhythm in the model light-organ symbiosis between
- Award ID(s):
- 1828262
- Publication Date:
- NSF-PAR ID:
- 10198203
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 117
- Issue:
- 44
- Page Range or eLocation-ID:
- p. 27578-27586
- ISSN:
- 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The binary association between the squid,
Euprymna scolopes , and its symbiont,Vibrio fischeri , serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, toV. fischeri is altered if the symbiont is removed from the light organ, suggesting that host colonization alters hemocyte recognition ofV. fischeri . To investigate the influence of symbiosis on immune maturation during development, we characterized hemocyte binding and phagocytosis ofV. fischeri and nonsymbioticVibrio harveyi from symbiotic (sym) and aposymbiotic (apo) juveniles, and wild‐caught and laboratory‐raised sym and apo adults. Our results demonstrate that while light organ colonization byV. fischeri did not alter juvenile hemocyte response, these cells bound a similar number ofV. fischeri andV. harveyi yet phagocytosed onlyV. harveyi . Our results also indicate that long‐term colonization altered the adult hemocyte response toV. fischeri but notV. harveyi . All hemocytes from adult squid, regardless of apo or sym state, both bound and phagocytosed a similar number ofV. harveyi while hemocytes from both wild‐caught and sym‐raised adults bound significantly fewerV. fischeri , although moreV. fischeri were phagocytosed by hemocytes from wild‐caught animals. In contrast, hemocytes from apo‐raised squid bound similar numbers of bothV. fischeri andV. harveyi , although moreV. harveyi cells were engulfed, suggesting that blood cellsmore » -
Microbes have been critical drivers of evolutionary innovation in animals. To understand the processes that influence the origin of specialized symbiotic organs, we report the sequencing and analysis of the genome of
Euprymna scolopes , a model cephalopod with richly characterized host–microbe interactions. We identified large-scale genomic reorganization shared betweenE. scolopes andOctopus bimaculoides and posit that this reorganization has contributed to the evolution of cephalopod complexity. To reveal genomic signatures of host–symbiont interactions, we focused on two specialized organs ofE. scolopes : the light organ, which harbors a monoculture ofVibrio fischeri , and the accessory nidamental gland (ANG), a reproductive organ containing a bacterial consortium. Our findings suggest that the two symbiotic organs withinE. scolopes originated by different evolutionary mechanisms. Transcripts expressed in these microbe-associated tissues displayed their own unique signatures in both coding sequences and the surrounding regulatory regions. Compared with other tissues, the light organ showed an abundance of genes associated with immunity and mediating light, whereas the ANG was enriched in orphan genes known only fromE. scolopes . Together, these analyses provide evidence for different patterns of genomic evolution of symbiotic organs within a single host. -
Abstract Increased exposure to light pollution perturbs physiological processes through misalignment of daily rhythms at the cellular and tissue levels. Effects of artificial light-at-night (ALAN) on diel properties of immunity are currently unknown. We therefore tested the effects of ALAN on diel patterns of cytokine gene expression, as well as key hormones involved with the regulation of immunity, in zebra finches (
Taeniopygia guttata ). Circulating melatonin and corticosterone, and mRNA expression levels of pro- (IL-1β ,IL-6 ) and anti-inflammatory (IL-10 ) cytokines were measured at six time points across 24-h day in brain (nidopallium, hippocampus, and hypothalamus) and peripheral tissues (liver, spleen, and fat) of zebra finches exposed to 12 h light:12 h darkness (LD), dim light-at-night (DLAN) or constant bright light (LLbright). Melatonin and corticosterone concentrations were significantly rhythmic under LD, but not under LLbright and DLAN. Genes coding for cytokines showed tissue-specific diurnal rhythms under LD and were lost with exposure to LLbright, exceptIL-6 in hypothalamus and liver. In comparison to LLbright, effects of DLAN were less adverse with persistence of some diurnal rhythms, albeit with significant waveform alterations. These results underscore the circadian regulation of biosynthesis of immune effectors and imply the susceptibility of daily immune and endocrine patterns to ALAN. -
Abstract The temporal niche that an animal occupies includes a coordinated suite of behavioral and physiological processes that set diurnal and nocturnal animals apart. The daily rhythms of the two chronotypes are regulated by both the circadian system and direct responses to light, a process called masking. Here we review the literature on circadian regulations and masking responses in diurnal mammals, focusing on our work using the diurnal Nile grass rat (
Arvicanthis niloticus ) and comparing our findings with those derived from other diurnal and nocturnal models. There are certainly similarities between the circadian systems of diurnal and nocturnal mammals, especially in the phase and functioning of the principal circadian oscillator within the hypothalamic suprachiasmatic nucleus (SCN ). However, the downstream pathways, direct or indirect from theSCN , lead to drastic differences in the phase of extra‐SCN oscillators, with most showing a complete reversal from the phase seen in nocturnal species. This reversal, however, is not universal and in some cases the phases of extra‐SCN oscillators are only a few hours apart between diurnal and nocturnal species. The behavioral masking responses in general are opposite between diurnal and nocturnal species, and are matched by differential responses to light and dark inmore »
