The cell biology and genome ofStentor pyriformis, a giant cell that embeds symbiotic algae in a microtubule meshwork
Authors: Boudreau Vincent , Albright Ashley R. , Gerbich Therese M. , Fadero Tanner , Yan Victoria , Larson Ben T. , Lucas-DeMott Aviva , Yung Jay , Moulin Solène L.Y. , Descovich Carlos Patiño , Slabodnick Mark M , Burlacot Adrien , Wang Jeremy R. , Niyogi Krishna K , Marshall Wallace F. 
Published: December 2024

AbstractEndosymbiotic events in which an endosymbiont is retained within a cell that remains capable of phagocytosis, a situation known as mixotrophy, provide potentially important clues about the evolutionary origins of eukaryotes, particularly regarding the relative evolutionary sequence of phagocytosis and endosymbiosis. Mixotrophy in ciliates is commonplace, but has been investigated at a cellular and molecular level almost entirely in one organism,Paramecium bursaria. Reliance on just one model system makes it difficult to know which cell biological aspects of this system represent general features of ciliate mixotrophy versus accidental features of the specific organism. Here we describe the cell biology and genome of the giant heterotrichous ciliateStentor pyriformis. We show that this giant unicellular organism containsChlorella variabilisas its endosymbiont, that theChlorellacan live freely outside the host, that within the host theChlorellacells are docked near the cell surface, surrounded by microtubule “baskets”, and that the photosynthetic efficiency of theChlorellais reduced inside theStentorcell compared to when it is free-living outside the host, with photon energy instead being shunted to non-photochemical quenching. Compared to the non-mixotrophicStentor coeruleus,S. pyriformishas several distinct cellular features that may be related to endosymbiosis: the presence of microtubule baskets, which are absent inS. coeruleus; positive rather than negative phototaxis, which is likely an adaptation to allow the photosynthetic symbionts access to sufficient light; and a lack of pigment in the host cell, which may be an adaptation to tolerate high light levels. Compared toP. bursaria,S. pyriformishas several similar cellular features: in both organisms, the symbiont is a strain ofChlorella variabilis; theChlorellaendosymbiont retains the ability to live freely when separated from the host; and the algal symbionts contained in perialgal vesicles are docked at the cell surface. One potentially informative difference betweenP. bursariaandS. pyriformisis thatS. pyriformisemploys a standard genetic code, similar to otherStentorspecies but different from most other ciliates, includingP. bursaria, which use a non-standard code in which one or more stop-codons are respecified to encode amino acids. This difference in genetic code could serve as a barrier to impede gene transfer from symbiont to host in other ciliates, but this would not be a factor inS. pyriformis. A second cell biological difference is that whereasP. bursariaperforms phototaxis by a kinetic accumulation mechanism, in which swimming is non-directional but cells slow down in regions of higher light intensity,S. pyriformisperforms directed swimming towards the direction of high light intensity. However, as inP. bursaria, phototaxis inS. pyriformisrequires the presence of theChlorella, implying a potential flow of information from the symbiont to direct the orientation and swimming of the host cell. We propose thatS. pyriformiswill serve as a useful model system for studying the evolution of mixotrophy and endosymbiosis, with unique advantages in terms of size and regenerative ability as well as distinct cellular and genomic features compared with other mixotrophic ciliate models.