Focus
Photosymbiosis in green algae: Diversity and its impacts on host and symbiont fitness
2025 Volume 90 Issue 3 Pages 147-151
Details
2025 Volume 90 Issue 3 Pages 147-151
Photosymbiosis is a symbiotic relationship between microalgae and non-photosynthetic eukaryotes. Such associations have independently evolved multiple times across a wide range of eukaryotic lineages. In some photosymbiotic relationships, photosymbionts supply photosynthetic products to the host, and, on the other hand, host organisms supply some nutrients. Considering these trophic interactions, photosymbiosis appears to be mutualistic, but the balance between benefits and costs is highly dependent on environmental conditions. In this article, we focus on photosymbioses in green algae, which show particularly high diversity in both symbiont and host species, and discuss how these symbiotic relationships affect the fitness of symbionts and their hosts.
The symbiotic relationships between microalgae and non-photosynthetic eukaryotes are collectively referred to as photosymbiosis, which has been identified patchily on the phylogenetic tree of a wide range of eukaryotic lineages. Symbionts include green algae, red algae, dinoflagellates, and diatoms, while host organisms include cnidarians, ciliates, dinoflagellates, amoebozoans, foraminiferans, heliozoans, acoels, and even vertebrates (more specifically, amphibians). Among these, green algae are known as one of the most diverse groups of symbiotic microalgae, with symbiotic partners spanning ciliates, cnidarians, amphibians, and amoebozoans (Fig. 1A). Photosymbiosis induces physiological and ecological changes in both symbionts and hosts through metabolic exchanges and cellular-level interactions. Such changes are thought to contribute to the colonization of new ecological niches, such as oligotrophic environments, and to the expansion of survival strategies. Although these relationships may appear mutually beneficial at first glance, recent studies have shown that the effects of photosymbiosis can vary greatly depending on environmental conditions, as well as the phylogenetic lineages of the hosts and symbionts. In photosymbioses involving green algae, the association benefits either the symbiont or the host, or both, under certain environments; however, changes in external conditions such as light or nutrient availability can impose costs on the organisms. Understanding how photosymbiosis influences the fitness of symbiotic algae, host organisms, or the entire symbiotic system—conceptualized as a holobiont—provides important insight into the evolutionary question of why photosymbioses have been adopted by such a wide range of organisms and maintained over long evolutionary timescales. In this article, we focus on photosymbiosis involving three classes of green algae (Trebouxiophyceae, Chlorophyceae, Chlorodendrophyceae), which exhibit particularly high diversity in their symbiotic associations, and review the known effects of environmental conditions and phylogenetic contexts on host and symbiont fitness.
(A) Diversity of green algal symbionts and their hosts. The classification of green algae is based on Baudelet et al. 2017. (B) A model of the effect of green algal photosymbionts on the host fitness. The photosymbionts generally support their hosts’ growth and survival, especially under starvation conditions.
The family Chlorellaceae consists of the Chlorella clade and Parachlorella clade, and photosymbiotic species are found in the former clade. Some species belonging to the genus Chlorella form symbiotic relationships with hydras (Hydra viridissima), ciliates (Paramecium bursaria, Stentor pyriformis), heliozoans (Acanthocystis turfacea), and amoebozoans (Mayorella viridis) (Luo et al. 2010; Kobayakawa 2017; Hoshina et al. 2021; Yamagishi et al. 2025). It is also known that some members of mixotrophic testate amoebae, a heterogenetic group including amoebozoans, rhizarians, and stramenopiles, harbor green algal symbionts. Gomaa et al. (2014) showed that, in the limited number of species examined, their symbionts constitute a single phylogenetic clade within the genus Chlorella. Some species in the genus Micractinium are also found as the photosymbionts of ciliates (P. bursaria, Tetrahymena utriculariae, Coleps viridis). All of them are endosymbionts, i.e., internalized in the host cells.
The Chlorella symbiont is thought to primarily provide photosynthetically fixed carbon, as a form of sugar such as maltose, to the host organism, while the host supplies nitrogen sources, such as amino acids, to the symbiont (Hamada et al. 2018; Jenkins 2024). Although this relationship was generally thought to be mutually beneficial, the effect of the symbiosis on the fitness of either the algal symbiont or the host organism has turned out to be greatly influenced by environmental conditions. In the P. bursaria–Chlorella symbiotic system, Lowe et al. (2016) suggested that host fitness varies significantly depending on light and nutrient conditions. Maintaining symbionts within host cells under dark conditions imposes additional costs on the hosts, negatively affecting its growth, and symbiont-free host cells exhibit higher fitness under such conditions. As light intensity increases, the growth rate of hosts harboring symbionts increases monotonically, and the net benefit of symbiosis to the host reaches its maximum under oligotrophic and high-light conditions. On the other hand, the growth rate of symbionts increases monotonically with light intensity in the free-living state, whereas it peaks under intermediate light conditions in the symbiotic state. Photosynthetic efficiency was also shown to decrease in the symbiotic state. Under dark conditions, the growth rate of symbiotic algae exceeds that of free-living ones. These results suggest that the symbiotic state is consistently costly for the symbiont and that the photosymbiosis observed in Paramecium bursaria represents a host-driven exploitative relationship (Lowe et al. 2016).
Such environment-dependent effects of photosymbiosis with Chlorella on host and symbiont fitness have also been investigated in other host organisms. In the cnidarian Hydra viridissima (green hydra), symbiotic individuals exhibit higher growth rates than aposymbiotic ones, and it has been shown that the symbionts enhance glycogen storage in the host and support host survival under starvation conditions (Muscatine and Lenhoff 1965; Cook and Kelty 1982; Hamada et al. 2018). The symbiotic Chlorella influences oogenesis in H. viridissima and is vertically transmitted through both asexual and sexual reproduction (Habetha et al. 2003; Kawaida et al. 2013). Furthermore, the Chlorella strain A99, a symbiont of H. viridissima, that proliferates intracellularly in the host cannot be permanently cultured outside of the host tissues (Hamada et al. 2018). These suggest that A99 may be an obligate symbiont of H. viridissima and depend on unknown host-derived factors necessary for its growth (Hamada et al. 2018).
In the photosymbiotic amoeba M. viridis, there is no significant difference in host growth rate between symbiotic and aposymbiotic states under conditions with sufficient prey. However, under starvation conditions, the survival of M. viridis is supported by the symbiotic Chlorella, indicating an influence on host fitness (Yamagishi et al. 2025). It remains unknown how general and common the phenomena observed in P. bursaria, H. viridissima, and M. viridis are.
Though many of the algal endosymbionts of sea anemones are dinoflagellates in the family Symbiodiniaceae, Trebouxiophyceae green algae within the genus Eliptochloris have symbiotic relationships with some sea anemones (Anthopleura elegantissima and Anthopleura xanthogrammica) and are known to be relatively close to lichens’ algal symbionts (Lewis and Muller-Parker 2004; Lestsch et al. 2009). Within the Chlorophyta, lichen symbionts are found principally in the classes Trebouxiophyceae and Ulvophyceae (Muggia et al. 2017; Martínez-Alberola et al. 2020; Sanders and Masumoto 2021). A study on Elliptochloris marina and its sea anemone host A. elegantissima has shown that symbiosis with this algal species suppresses body mass loss of the host and increases the frequency of asexual reproduction (Bingham et al. 2014). Additionally, compared to aposymbiotic individuals, those harboring E. marina were more frequently observed to possess well-developed gonads (Bingham et al. 2014). These findings suggest that E. marina contributes to enhancing the fitness of its sea anemone host (Bingham et al. 2014).
Symbionts in the order Chlamydomonadales belonging to two distinct genera (Oophila in Stephanospherinia and Chlorococcum in Moewusinia) are found inside their egg masses of some amphibian species (Rana [frogs], Ambystoma, and Hynobius [salamanders]) (Vences et al. 2024). The symbiotic algae residing within the egg capsule are thought to supply photosynthetic products and oxygen to the host embryo, while the host provides ammonia as a nitrogen source to the symbiotic algae (Graham et al. 2013; Small et al. 2014). In the symbiosis between salamanders and Chlamydomonadales, the symbiotic algae are shown to contribute to the host’s fitness. Particularly during the embryonic developmental stages of the host salamander, the symbiotic algae play an important role, with reports showing that the algae increase the embryo’s survival rate, hatching success, and even the speed of hatching (Gilbert 1944; Tattersall and Spiegelaar 2008). Additionally, it has been reported that during symbiosis with the host A. maculatum, part of the algal population of O. amblystomatis is taken up into the host’s cells (Burns et al. 2017). The internalized algal cells are suggested to experience multiple stresses within the host cells, such as hypoxic stress and sulfur starvation. On the other hand, the host cells may gain nutritional benefits from the algal cells while maintaining them intracellularly by suppressing their own immune regulatory factors (Burns et al. 2017). As mentioned above, the symbiotic algae of amphibians are mainly classified into two groups, but to what extent and which group affects host fitness remains largely unknown. Therefore, in future physiological and ecological studies, it is critical to take into account the varieties and compositions of symbiotic algae.
Some Chlamydomonadales species form symbiotic relationships with certain large benthic foraminiferans (LBF) (Androsina, Archaias, Broeckina, Cyclorbiculina, Laevipeneroplis, Parasorites), although the phylogenetic positions of the symbionts are not fully characterized. Phylogenetic analysis by Pawlowski et al. (2001) suggested that the symbiotic Chlamydomonadales species form a single clade closely related to Chlamydomonas noctigama. The influence of Chlamydomonadales symbiotic algae on the fitness of their LBF hosts is mostly unknown. Meanwhile, among LBF, there are reports on the effects of photosymbiosis on host fitness in Amphistegina lobifera, which hosts diatoms, and Sorites orbiculus, which hosts dinoflagellates (Schmidt et al. 2025). Schmidt et al. (2025) compared artificially induced aposymbiotic hosts with symbiotic ones and found that the motility and growth rates of the hosts were reduced in the aposymbiotic state. Schmidt et al. (2025) conclude that it remains unclear whether this fitness decline is due to the chemical treatment used to induce aposymbiotic states or the absence of the symbionts. The difficulty in separately evaluating the effects of chemical treatment and the absence of symbiotic algae may stem from the inability to maintain and culture aposymbiotic LBF continuously in laboratory conditions, requiring phenotypic observations immediately after chemical treatment. Compared to other symbiotic systems, information on the effects of photosymbiosis on the holobiont fitness of LBF is particularly limited. One cause may be that many LBF species cannot be maintained through successive culture in laboratory environments. Establishing stable successive culture systems for multiple species is important for the advancement of photosymbiosis research in LBF.
Many algal species that belong to the genus Tetraselmis within the class Chlorodendrophyceae have been reported to form symbiotic relationships with acoels (Riewluang and Wakeman 2023). Tetraselmis species symbiotic with acoels are broadly distributed in the phylogenetic tree and classified into four clades (Riewluang and Wakeman 2023). Among these, the symbiosis between Tetraselmis convolutae and the acoel Symsagittifera roscoffensis has been studied particularly extensively. The symbiosis with T. convolutae is essential for the acoel host to mature into an adult. The acoel larvae hatched from non-symbiotic eggs cannot survive unless they establish symbiosis with T. convolutae (Keeble and Gamble 1907; Oschman 1966). On the other hand, T. convolutae is capable of proliferating outside the host, suggesting that the degrees of dependency on the symbiosis and their effects on fitness greatly differ between the host and symbiont.
As we have reviewed so far, although photosymbiosis may appear to be a mutually beneficial relationship at first glance, its actual effects on the fitness of both hosts and symbionts are highly dependent on environmental conditions. Thus, simply characterizing it as mutualism could be misleading: In some cases, the relationship may incur costs for both partners. Such environment-dependent effects on fitness have been reported primarily in photosymbiotic systems involving Chlorellaceae (Muscatine and Lenhoff 1965; Lowe et al. 2016; Yamagishi et al. 2025). In particular, the positive impact of symbiosis on host fitness under starvation conditions has been observed across different host species, suggesting a certain degree of generality in the fitness effects of photosymbiosis (Fig. 1B). Therefore, when evaluating the overall fitness consequences of symbiotic associations, it is essential to consider the combined effects of environmental factors such as light intensity and nutrient availability, and to assess both the benefits and costs of photosymbiosis. Additionally, in symbioses involving other Trebouxiophyceae and Chlamydomonadales algae with diverse hosts—including cnidarians, acoels, and amphibians—photosymbiosis has been shown to affect the host reproduction, development, and survival (Keeble and Gamble 1907; Gilbert 1944; Oschman 1966; Tattersall and Spiegelaar 2008; Bingham et al. 2014). The balance between the benefits and costs of green algal photosymbiosis represents a complex structure determined by the combination of host, symbiont, and environmental factors. Comprehensive studies across a broader range of taxa, beyond a few model systems, will be crucial for achieving a more generalized understanding of the evolutionary and ecological significance of photosymbiosis.
We thank Colin J. Anthony for his help in illustrating the salamander egg. This work was supported by JST SPRING, Grant Number JPMJSP2108 and JSPS KAKENHI Grant Numbers 24KJ0740 (to D. Y.), JSPS KAKENHI 23H04962, 24H01462, 25K02339 (to S. M.).
