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<p>When in symbiosis, <i>Gerakladium spongiolum</i> are Symbiodiniaceae dinoflagellates that occupy symbiosomes within the cells of the host sponge <i>Cliona varians</i>. These symbionts enhance rates of growth and bioerosion of the host, and the symbiosis is remarkably resistant to environmental stressors. Intracellular Symbiodiniaceae symbionts like <i>G. spongiolum</i> experience drastically different conditions within the host cell organelle compared to the environment outside of the cell. We need a better understanding of adaptations that may permit long-term intracellular residency in symbioses involving Symbiodiniaceae, including those that that are related to chronobiological stressors. To better understand aspects of this resilient partnership from the symbiont’s perspective, we examined structures within <i>Gerakladium</i> cells over the course of a 24-h day:light cycle. We sampled sponge tissue at four time points: 06:00 (shortly before sunrise), 12:00 (near solar maximum), 18:00 (≈ 2&#xa0;h before sunset), and at 00:00. Tissue from each time point was fixed for transmission electron microscopy. No diel changes were observed in total planar surface area of the algal cells found within sponge cells. The surface area of chloroplasts and pyrenoids, however, changed throughout the 24-h sampling period peaking at 12:00 and 18:00, respectively. Additionally, the thickness of the peri-pyrenoidal carbohydrate plates changed throughout the course of a day:night cycle as did the number of electron-dense and electron-sparse granules. While not related to the circadian patterns we examined, live sponge tissue was used to qualitatively assess the pH of the symbiosome using confocal microscopy. The pH of the symbiosome was below 4 in the tissue we examined. Our results demonstrate that the organelles are an acidified environment for the dinoflagellate, which differs from the environment they experience when they are free-living, and that some of the photosynthetic machinery and other subcellular elements respond dynamically throughout a 24-h cycle. We suggest these are part of a comprehensive adaptive strategy that permits long-term residency within the host cell by the symbiont. It remains to be seen whether these observations apply to non-sponge symbioses.</p> Graphical abstract <p>Over the course of a day-light cycle, the surface area of <i>Gerakladium spongiolum</i> cells did not change but the surface areas of chloroplasts and pyrenoids did change throughout the day. Subcellular granules also demonstrated diel changes in surface area and number. The potential role these changes as a strategy for long-term residence of Symbiodiniaceae within heterotrophic host cells is discussed.</p>

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Diel changes in subcellular traits of an intracellular Symbiodiniaceae sponge specialist: pyrenoid, chloroplast, and granule plasticity in the symbiont Gerakladium spongiolum

  • 期刊论文

  • 发表日期：

    2025年8月14日

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  • Rachel DuMez-Kornegay,
  • Christine Lacy,
  • Malcolm Hill

摘要

When in symbiosis, Gerakladium spongiolum are Symbiodiniaceae dinoflagellates that occupy symbiosomes within the cells of the host sponge Cliona varians. These symbionts enhance rates of growth and bioerosion of the host, and the symbiosis is remarkably resistant to environmental stressors. Intracellular Symbiodiniaceae symbionts like G. spongiolum experience drastically different conditions within the host cell organelle compared to the environment outside of the cell. We need a better understanding of adaptations that may permit long-term intracellular residency in symbioses involving Symbiodiniaceae, including those that that are related to chronobiological stressors. To better understand aspects of this resilient partnership from the symbiont’s perspective, we examined structures within Gerakladium cells over the course of a 24-h day:light cycle. We sampled sponge tissue at four time points: 06:00 (shortly before sunrise), 12:00 (near solar maximum), 18:00 (≈ 2 h before sunset), and at 00:00. Tissue from each time point was fixed for transmission electron microscopy. No diel changes were observed in total planar surface area of the algal cells found within sponge cells. The surface area of chloroplasts and pyrenoids, however, changed throughout the 24-h sampling period peaking at 12:00 and 18:00, respectively. Additionally, the thickness of the peri-pyrenoidal carbohydrate plates changed throughout the course of a day:night cycle as did the number of electron-dense and electron-sparse granules. While not related to the circadian patterns we examined, live sponge tissue was used to qualitatively assess the pH of the symbiosome using confocal microscopy. The pH of the symbiosome was below 4 in the tissue we examined. Our results demonstrate that the organelles are an acidified environment for the dinoflagellate, which differs from the environment they experience when they are free-living, and that some of the photosynthetic machinery and other subcellular elements respond dynamically throughout a 24-h cycle. We suggest these are part of a comprehensive adaptive strategy that permits long-term residency within the host cell by the symbiont. It remains to be seen whether these observations apply to non-sponge symbioses.

Graphical abstract

Over the course of a day-light cycle, the surface area of Gerakladium spongiolum cells did not change but the surface areas of chloroplasts and pyrenoids did change throughout the day. Subcellular granules also demonstrated diel changes in surface area and number. The potential role these changes as a strategy for long-term residence of Symbiodiniaceae within heterotrophic host cells is discussed.