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1. Stability of the cnidarian–dinoflagellate symbiosis is primarily determined by symbiont cell-cycle arrest

   https://doi.org/10.1073/pnas.2412396122  

   Gorman, Lucy M; Tivey, Trevor R; Raymond, Evan H; Ashley, Immy A; Oakley, Clinton A; Grossman, Arthur R; Weis, Virginia M; Davy, Simon K (April 2025, Proceedings of the National Academy of Sciences)

   Queller, David (Ed.)

   The cnidarian–dinoflagellate symbiosis relies on the regulation of resident symbiont populations to maintain biomass stability; however, the relative importance of host regulatory mechanisms [cell-cycle arrest (CC), apoptosis (AP), autophagy (AU), and expulsion (EX)] during symbiosis onset and maintenance is largely unknown. Here, we inoculated a symbiont-free (aposymbiotic) model cnidarian (Exaiptasia diaphana: “Aiptasia”) with either its native symbiont Breviolum minutum or one of three non-native symbionts: Symbiodinium microadriaticum, Cladocopium goreaui, and Durusdinium trenchii. We then measured and compared host AP, host AU, symbiont EX, and symbiont cell-cycle phase for up to a year with these different symbionts and used these discrete measurements to inform comparative models of symbiont population regulation. Our models showed a general pattern, where regulation through AP and AU is reduced after onset, followed by an overshoot of the symbiont population that requires a strong regulatory response, dealt with by strong CC and increased EX. As colonization progresses into symbiosis maintenance, CC remains crucial for achieving steady-state symbiont populations, with our models estimating that CC regulates 10-fold more cells (60 to 90%) relative to the other mechanisms. Notably though, our models also revealed that D. trenchii is less tightly regulated than B. minutum, consistent with D. trenchii’s reputation as a suboptimal partner for this cnidarian. Overall, our models suggest that single regulatory mechanisms do not accurately replicate observed symbiont colonization patterns, reflecting the importance of all mechanisms working concomitantly. This ultimately sheds light on the cell biology underpinning the stability of this ecologically significant symbiosis. 

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2. Co-infesting symbionts on a threatened marine host: evaluating correlations between an introduced parasitic isopod and a native symbiotic clam

   https://doi.org/10.3354/meps14105  

   Li, J.; Chapman, J.; Johnson, P. (January 2022, Marine ecology)

   In marine ecosystems, increased global-scale transportation creates opportunities for rapid introduction of invasive parasitic species that, in some cases, result in dramatic shifts within the native communities. A lack of detailed knowledge regarding the ecology of invasive marine parasites hinders our ability to develop effective conservation strategies and avoid unforeseen ecological consequences. We examined co-infestation patterns of a highly pathogenic, introduced parasitic isopod (Orthione griffenis) and a native symbiotic clam (Neaeromya rugifera) on the North American native blue mud shrimp Upogebia pugettensis. Our comparisons included infestations of O. griffenis and N. rugifera among 447 U. pugettensis hosts over 3 study years and were designed to statistically assess whether the 2 symbionts exhibited significant associations with one another. Our results indicate that infestations by the 2 symbiont species are positively correlated, such that the presence of one symbiont is a strong, positive predictor for the presence of the other. For both symbionts, host size is an important factor that drives the observed correlation. Host sex is also influential for O. griffenis. Interestingly, even after accounting for these host attributes, the infestations by the 2 symbionts continue to correlate positively, particularly among older (second-year and beyond) symbionts, highlighting the likely influence of additional host and environmental factors in driving the symbiont correlation post-settlement. We consider potential mechanisms, including differential energetic reserves and longevities between infested and co-infested hosts, in detail. These results offer insights into the ecological drivers of symbiont co-infestation, which have important implications for understanding host-parasite interactions and future conservation measures. 

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3. Comparative physiology reveals heat stress disrupts acid-base homeostasis independent of symbiotic state in the model cnidarian Exaiptasia diaphana

   https://doi.org/10.1242/jeb.246222  

   Allen-Waller, Luella; Jones, Katelyn G.; Martynek, Marcelina P.; Brown, Kristen T.; Barott, Katie L. (January 2024, Journal of Experimental Biology)

   Climate change threatens symbiotic cnidarians’ survival by causing photosymbiosis breakdown in a process known as bleaching. Direct effects of temperature on cnidarian host physiology remain difficult to describe because heatwaves depress symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system to disentangle direct vs. indirect heat effects on the host, since it can survive indefinitely without symbionts. We tested the hypothesis that heat directly impairs cnidarian physiology by comparing symbiotic and aposymbiotic individuals of two laboratory subpopulations of a commonly used clonal strain of E. diaphana, CC7. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C, +6°C) for 15–18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration, and host intracellular pH (pHi). Symbiotic anemones from the two subpopulations differed in size and symbiont density and exhibited distinct heat stress responses, highlighting the importance of acclimation to different laboratory conditions. Specifically, the cohort with higher initial symbiont densities experienced dose-dependent symbiont loss with increasing temperature and a corresponding decline in host photosynthate accumulation. In contrast, the cohort with lower initial symbiont densities did not lose symbionts or assimilate less photosynthate when heated, similar to the response of aposymbiotic anemones. However, anemone pHi decreased at higher temperatures regardless of cohort, symbiont presence, or photosynthate translocation, indicating that heat consistently disrupts cnidarian acid-base homeostasis independent of symbiotic status or mutualism breakdown. Thus, pH regulation may be a critical vulnerability for cnidarians in a changing climate. 

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4. Interactions of Symbiotic Partners Drive the Development of a Complex Biogeography in the Squid-Vibrio Symbiosis

   https://doi.org/10.1128/mBio.00853-20  

   Essock-Burns, Tara; Bongrand, Clotilde; Goldman, William E.; Ruby, Edward G.; McFall-Ngai, Margaret J.; Graf, Joerg (June 2020, mBio)

   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. fischeri - produced bioluminescence, but it does require metabolically active symbionts. Further, while symbionts in the most mature crypts have a higher proportion of live cells and a greater likelihood of expulsion at dawn, they have a lower resistance to antibiotics. The overall dynamics of these distinct microenvironments reflect the complexity of the host-symbiont dialogue. IMPORTANCE The complexity, inaccessibility, and time scales of initial colonization of most animal microbiomes present challenges for the characterization of how the bacterial symbionts influence the form and function of tissues in the minutes to hours following the initial interaction of the partners. Here, we use the naturally occurring binary squid-vibrio association to explore this phenomenon. Imaging of the spatiotemporal landscape of this symbiosis during its onset provides a window into the impact of differences in both host-tissue maturation and symbiont strain phenotypes on the establishment of a dynamically stable symbiotic system. These data provide evidence that the symbionts shape the host-tissue landscape and that tissue maturation impacts the influence of strain-level differences on the daily rhythms of the symbiosis, the competitiveness for colonization, and antibiotic sensitivity. 

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5. How host-microbiome/holobiont evolution depends on whether the microbiome affects host lifespan or fecundity

   https://doi.org/10.1093/jeb/voae127  

   Brown, Alexandra L; Koskella, Britt; Boots, Mike (January 2025, Journal of Evolutionary Biology)

   Li_Richter, Xiang-Yi; Jain, Kavita (Ed.)

   Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

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