Vegetative cell fusion and a new stage in the life cycle of the Aphelida (Opisthosporidia)

doi:10.21203/rs.3.rs-1980474/v1

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Vegetative cell fusion and a new stage in the life cycle of the Aphelida (Opisthosporidia)

https://doi.org/10.21203/rs.3.rs-1980474/v1

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The aphelids, intracellular parasitoid of algae, play significant role in the ponds communities regulating the algae blooms. They represent a large cluster of OTUs sister to Fungi at the molecular phylogenetic tree sharing a common ancestor with fungi. Their vegetative life cycle being similar to that of chytridiomycetes includes opisthokont uniflagellar zoospores, cysts, phagotrophic intracellular stage, and multinuclear plasmodium producing zoospores. The sexual part of life cycle is not known, and, as we can see now, the asexual part is also understudied. We have found in the Aphelidium insulamus and other ahelid species a new stage – big multiflagellar, or amoeboid cells, which can be considered both, the result of zoospore fusion, or the remnant of plasmodium after zoospore formation. A study of this phenomenon lead us to the conclusion, that after multicellular infection the trophic stages of different parasitoids fuse in one plasmodium having different sorts of nuclei. Some of them become the nuclei of zoospores, while the others left in the remnant of plasmodium, which becomes a monster. The families of protein encoded genes involved in the vegetative cell fusion was also discussed.

Cell Cycle & Proliferation

Aphelidiomycota

plasmodium

zoospores

monsters

cell fusion

The aphelids, parasitoids of fresh-water and marine algae, are known from the 19th century (Cienkowski 1865, Zopf 1885, 1887, de Bruyne 1890, Dangeard 1890, Scherffel 1925). The increasing of their study has been occurred twice: by electron microscopy (Gromov and Mamkaeva 1970a-c, 1975, Schnepf et al. 1971, Schnepf 1972, 1974, Gromov 1972, 1976, 2000, Schweikert and Schnepf 1996, 1997) and molecular phylogeny (Karpov et al. 2013, 2014a,b, 2016, 2017a,b, 2019, Letcher et al. 2013, 2015, 2017, Torruella et al. 2018, Tcvetkova et al. 2019, Seto et al. 2020, 2022, Pozdnyakov et al. 2021). Two recent investigation pikes have been caused by the same reason: massive death of algal cultures from unknown agent in the lab (Gromov and Mamkaeva 1966) and in the open ponds for fuel industry (Letcher et al. 2013).

The asexual stages of life cycle are well known for all aphelids: they include a zoospore forming a cyst on the host cell, which inject trophic amoeba in the host; amoeba phagocytizes the host cell contents and becomes a multinuclear plasmodium, which produces zoospores (Fig. 1). Sexual stages are unknown for the aphelids (e.g. Gromov 2000, Karpov et al. 2014). We have never seen gametes and zygotes of the aphelids although they should be there because the genes of meiotic and other connected to sexual stages proteins are present in the Paraphelidium, Amoeboaphelidium and Aphelidium transcriptomes (Torruella et al. 2018, Galindo et al. 2022) and genomes (Mikhailov et al. 2022, submitted). Therefore, we are not sure that the described life cycle of the aphelids is complete.

Here we demonstrate at the light microscopic level the unusual multiflagellated and amoeboid stages in the strains of Aphelidium insulamus and Aph. melosirae parasitizing Tribonema gayanum, Amoeboaphelidium protococcorum and Am. chlorellavorum on Scenedesmus obliquus, cell fusion in their life cycle, and discuss the distribution of cell fusion proteins in the aphelids and other holomycotans.

Strains X-102 of Aphelidium melosirae Scherffel 1925, X-133 and X-134 of Aph. insulamus Karpov, Zorina et Moreira 2020 from the Culture Collection of Parasitic Protists (CCPP) ZIN RAS were cultivated as it was written elsewhere (Karpov et al. 2020). Cells with two or more flagella were observed during massive release of zoospores. The single cell PCR and following 18S rRNA gene sequencing of strain X-133 has been done according to earlier published protocol (Karpov et al. 2020).

I – cyst (cy) injected its contents (tr) in the host cytoplasm (hc). II – trophont (tr) grows and becomes multinuclear (n) plasmodium (III) containing a vacuole with residual body (rb). IV – plasmodium divides into uninuclear cells – immature zoospores (iz). V – mature zoospores (zo) and residual body (rb) in empty host cell. VI – zoospores release to infect new cells of Tribonema.

The list of genes involved in the vegetative cell fusion was compiled based on the paper by Fischer and Glass (2019). The protein encoded gene sequences were download from the NCBI database and aligned on predicted proteomes of Paraphelidium tribonematis (https://doi.org/10.6084/m9.figshare.7339469.v1) and Amoeboaphelidium protococcorum (NCBI ID:114058) using blastp ncbi 2.12.0+. Alignment results analysis for searching the similarities in functional-active regions was carried out on the base of the descriptions of protein molecular structures in UniProt and NCBI databases. In addition, proteins of selected fungal genes and aphelid proteomes were analyzed using the Protheinortho v.6.1.0 (Lechner et al. 2011) to search for orthologs of fungal genes in the aphelids.

New forms (monsters) in the life cycle of Aphelidium spp.

The strain X-133 of Aphelidium insulamus has been originally established by the infection of its plasmodium the Tribonema gayanum culture. In the mature culture after several asexual cycles we found among typical uniflagellated zoospores the motile cells with two, three and more (up to 12) immotile flagella (Fig. 2A–C) called here the monsters. They are also opisthokonts, as the flagella are behind of the cell during their movement. The monsters are spherical and bigger (up to 10 µm diam.) than the uniflagellated zoospores (3 µm in length). They do not use their stiff flagella for the movement, but instead monsters craw using anterior pseudopodia.

Sometimes we observed amoeboid monsters without flagella, but producing rather long and branching filopodia (Fig. 2D). They were often found inside the empty host cell. These filopodia seem to be used for the movement also, as the cells can come out from the empty host cell moving like amoeba (Fig. 2E). Both types of monsters were very rare in the culture, and we were not able to study them in more details.

The single cell PCR of the monsters and following sequencing have shown, that the monsters have 18S rRNA gene identical to that of strain X-133 of Aph. insulamus (Fig. S1, S2). The multiflagellar monsters have been noted also in the strain X-102 of Aph. melosirae and X-134 of Aph. insulamus from aphelid collection (CCPP ZIN RAS).

Monsters in the life cycle of Amoeboaphelidium spp.

Similar stage in the aphelid life cycle has been observed by Gromov and Mamkaeva (1968) on Amoeboaphelidium protococcorum and Am. chlorellavorum, having amoeboid zoospores. The authors found among the usual zoospores of 2 µm in length a few giant amoebae from 3 to 5 times bigger and having from one to four nuclei. These large amoebae have already had several nuclei, before leaving a host cell after zoospore release. In other words, when zoospores release the host cell, the remnant of plasmodium representing non divided peace of parasitoid with several nuclei becomes active and also releases the host cell as a giant amoeba. The fate of such amoebae after releasing is questionable, although K.A. Mamkaeva (pers. communication) noticed, that after a short period of activity some monsters stop and die.

We also found the amoeboid monsters of Aphelidium spp. in the empty host cell after zoospore release, but they had no flagella, what is unusual for this genus. Probably, such amoeboid monsters become active before the formation of flagella, and were not able to build flagella afterall. Flagellated monsters, thus, represent more mature stage of the remnant of plasmodium however moving with pseudopodia anyway. Therefore, we suggest that the monster is the non-divided remnant plasmodium, which can be present in the host cell together with mature zoospores having flagella already (Fig. 2F). If so, the monsters make nothing with zoospore fusion.

Is there cell fusion in the aphelid life cycle?

At the same time, the multicellular infection, when single host cell is attacked by numerous zoospores, has been shown for all aphelids (Gromov and Mamkaeva 1968, 1970a-c, Gromov 1972, 2000, Karpov et al. 2013, 2014a, 2017a-c, Letcher et al. 2013, 2015, Schweikert and Schnepf 1996, Seto et al. 2020, 2022). It means that several parasitoids can penetrate the host and the trophonts develop separately inside the host cell. However, we always observe only one plasmodium producing zoospores independently of number of initial trophonts (i.e., Gromov and Mamkaeva 1970b). We have had evidences of two young trophonts developing in a host cell and their fusion in a plasmodiim with two still separate residual bodies in Paraphelidium letcheri (Karpov et al. 2017b – Fig. 2H and K) (Fig. 3,III).

Fusion of two separate cells in the host cell Scenedesmus obliquus has been described for Amoeboaphelidium protococcorum (Gromov and Mamkaeva 1968). Taking into account, that the strain X-133 of Aph. insulamus is a result of inoculation with plasmodium (see M&M), we can propose, that the trophont’s fusion could have place and the plasmodium already had two (at least) sorts of nuclei appeared from different zoospores. Probably, the nuclei of one parental zoospore only can produce another generation of zoospores, and the remnant of plasmodium becomes a monster, which cannot survive. However, the fusion of nuclei of two trophic cells of parasitoid is also possible, and in this case, we can interpret the monsters as containing somewhat pycnotic nuclei after meiotic divisions, which has to be removed in a form of monster.

Trophont’s fusion after multiple infection have been found in Aph. chlorococcorum by Gromov B.V. (pers. communication): trophozoites from several cysts infect the host cell (Scenedesmus) and develop independently. Then they fuse in a plasmodium, which produces zoospores. There were no monsters in this case, what can propose that all infecting zoospores belonged to the same strain of Aph. chlorococcorum.

Comparative molecular analysis

We undertook a comparative molecular analysis to investigate the possibility of vegetative cell fusion in aphelids, based on known data on aphelid-related opisthokonts.

The molecular mechanisms of cell fusion were studied in filamentous fungi, mainly in Neurospora crassa as the model object (Aguilar et al. 2013, Croll et al. 2009, Daskalov et al. 2017, Fischer and Glass 2019, Fu et al. 2011, Lechner et al. 2011, Read et al. 2010, Simonin et al. 2012) and some taxa of Metazoa (mostly the Mammalia, Insecta and Nematoda) (Aguilar et al. 2013, Dhanyasi et al. 2015, Gruenbaum-Cohen 2012, Hindi et al. 2013, Ishikawa et al. 2014, Podbilewicz et al. 2006, Smurova and Podbilewicz 2016 among others).

In filamentous fungi the vegetative cell fusion is the complex action where many wide-affecting regulatory systems are involved. According to sources for N. crassa vegetative cell fusion the common work of CWI (cell wall integrity) pathway and MAK-2 Signal Response pathway together with the STRIPAC (striatin-based) complex is required. Additionally, the phosphatase CSP-6 and WHI-2 protein interact with the STRIPAC complex, and the correct functioning of these genes is also required for vegetative cell fusion.

The effects on vegetative cell fusion in N. crassa were shown for NADPH-oxidase complex (NOX-1) (reactive oxygen species dependent signaling), orthologs of genes BemA, RacA, Cdc24, Cdc42 of Epichloe festucae (regulators of polarized growth and cytoskeletal dynamics), proteins related to actin-myosin system and actin regulations (Arp2/3 complex, CAP-1/CR-1 complex etc), gene amph-1 of N. crassa (BAR domain containing protein, involved in dynamics of membrane-cytoskeleton interaction), some membrane-embedded (ham-8, ham-9 of N. crassa) and membrane-affecting proteins (erg-2, prm-1, lfd-1, lfd-2, fig-1, NCU01697 of N. crassa), some other proteins participating in mentioned interactions.

In the search for homologs of 43 proteins corresponding to genes involved in cell fusion mechanisms in the predicted proteomes of Amoeboaphelidium protococcorum (Mikhailov et al. 2022, submitted) and Paraphelidium tribonematis (Torruella et al. 2018) for 19 genes were found the orthologs among the aphelid genes (Table 1, S1). For 15 genes the full orthologue was not determined but for the functional-active regions of proteins were found the homologic sites in the aphelid proteins. For 8 analyzed genes the accordance in the aphelids were not found. They are the cell wall integrity receptors, the mentioned membrane proteins, and one protein specific to fungi of the Ascomycota lineage.

These data reveal that filamentous fungi differ from the aphelids in membrane protein composition that is probably provides the osmotrophy and cell wall presence. At the same time the main fungal signaling pathways and molecular machineries work or could work in the aphelids.

Thus, one can propose that cell fusion by the “fungal mechanism” could be released in the aphelids with replace of fungal membrane proteins with some unknown aphelid specific ones. However, this possibility does not mean that this mechanism really takes place, because all cell fusion linked machineries are universal and can be involved in different fungal cell functions and processes. At the same time, we cannot ignore this possibility and have to estimate the presence of such protein encoded genes in the aphelids as a confirmation of cell fusion at the trophic stage of their life cycle described in the present paper in several species of three aphelid genera.

Our search for homologs of proteins participating in cell fusion in Metazoa (cadherins, EFF-1, RAB-5, DYNAMIN-1 and others) does not bring the positive results. Probably, the metazoan molecular pathways linked to cell fusion do not work in the aphelids. These pathways are either apomorphic for Metazoa and not rooted in molecular machinery of common opisthokont ancestor, or they were lost in the aphelids in their evolutionary history.

We can suggest that the fusion of two or more parasitoids is possible during plasmodium formation in the aphelids, and it regularly occurs in the cultures, and in the natural environments as well. When multinuclear plasmodium produces zoospores, part of it with several nuclei from zoospores of different strains, does not divide, produces filopodia or flagella, and becomes a monster. This is, probably, a reason of monsters appearing in the culture: nuclei in plasmodium segregate accordingly their origin and form two, or maybe more (depending of number of infecting trophonts) remnants of plasmodium. Their fate is unclear.

In any case, the cell fusion takes place in plasmodium formation after multiple infection and at least the cytoplasmic exchange between strains occurs. We know nothing about the fusion of nuclei in the aphelids, although some electron microscopic images show the close contact of several nuclei in Amoeboaphelidium protococcorum (Gromov and Mamkaeva 1968), which can be interpreted as the first stage of their fusion. Unfortunately, these data have been received using fixation with KMnO₄, which often gives essential artefacts in the cell structure.

Acknowledgements

We thank Maria Ciobanu for help to make the monster’s photos with 40x objective. This work was supported by RSF grant 21-74-20089, cultivation of the aphelids was supported by grant of the Ministry of Science and Higher Education of the Russian Federation 075-15-2021-1069.

Authors’ contributions

Victoria S. Tcvetkova performed culture cultivation and LM observations, and Natalia A. Zorina performed culture sequencing. Igor R. Pozdnyakov performed molecular analysis. Sergey A. Karpov conceptualized the manuscript. Sergey A. Karpov, Igor R. Pozdnyakov and Alexei O. Seliuk drafted and edited the manuscript.

Compliance with ethical standards

All authors are sure that all data and materials as well as software application or custom code support their published claims and comply with field standards.

Conflict of interest

The authors declare that they have no conflict of interest.

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