**12. Conclusions**

Meiotic sex appears to be a primordial characteristic of microbial eukaryotes and has likely provided a continuous adaptive benefit for as long as 1.5 billion years in diverse lineages of microbial eukaryotes. Since eukaryotes appear to have evolved from an archaeal ancestor, the adaptive function of sexual processes, even in archaeal species, is relevant to understanding sexual processes in microbial eukaryotes. In the archaea, homologous recombinational repair of DNA damages appears to be the principal adaptive benefit of sexual processes. Conclusions bearing on the adaptive benefit of sexual processes (syngamy and meiosis) in microbial eukaryotes are summarized below.

The dikaryotic fungi (*Ascomycetes* and *Basidiomycetes*) include some of the most well-studied microbial eukaryotic species with respect to sexual reproduction. Wallen and Perlin [76] concluded in a 2018 review of the function and maintenance of sexual reproduction in the dikaryotic fungi that sexual reproduction, including its central feature of homologous recombination, evolved to repair DNA damages that arise particularly from environmental stresses. In the ascomycete yeast *S. cerevisiae,* DNA repair by homologous recombination during mitosis is well established. Recombinational repair during meiosis is stimulated under starvation conditions and appears to be even more efficient than during mitosis. In natural populations of *S. cerevisiae* and *S. paradoxus*, the great majority of matings that occur are between

closely genetically related individuals. Thus sex in these species is unlikely to be primarily maintained by an adaptive benefit of producing genetic variation.

The ascomycete *S. pombe*, like *S. cerevisiae*, tends to mate when nutrients are scarce. Introduction of DNA damage by different DNA damaging conditions stimulates sexual reproduction and meiotic recombination, consistent with the idea that meiotic recombination is an adaptation for repair. Another ascomycete, *C. albicans* is regarded as a parasexual, rather than sexual, species since it appears to undergo a meiotic process that is not associated with the organized chromosome segregation that normally results in haploid meiotic products. Nevertheless *C. albicans* contains a set of genes homologous to genes that function in meiosis in other species including a key gene that only functions in meiosis. Same sex mating in *C. albicans* likely occurs frequently in nature especially under environmental stress conditions. *U. maydis* is a basidiomycete fungus. Upon infecting its plant host it can undergo meiosis. Recombinational repair occurring during meiosis likely helps protect the *U. maydis* genome from oxidative attack by the plant host's defensive system against invading fungal pathogens.

*Paramecium tetraurelia*, a unicellular ciliate, undergoes clonal aging over successive asexual generations leading eventually to extinction. However, if aging paramecia are allowed to undergo a sexual process, either conjugation (mating with another individual) or automixis (self-fertilization), the progeny have a lifespan characteristic of youthful paramecia. During clonal aging DNA damage dramatically increases. Presumably, during automixis or conjugation, age-related DNA damage is repaired by homologous recombination.

*Volvox carteri* is a facultatively sexual colonial green algae. Sex (syngamy and meiosis) can be induced by conditions that cause oxidative stress, suggesting that sex may be a response to oxidative DNA damage.

*T. brucei* is a trypanosome parasite that causes human sleeping sickness. The tsetse fly acts as a vector for transmitting the parasite. *T. brucei* after infecting the fly is able to undergo meiosis in the fly's salivary glands. The tsetse fly can defend itself against *T. brucei* infection, in part, by producing DNA damaging reactive oxygen species. When the trypanosomes within the fly's salivary glands undergo meiosis, the associated homologous recombination likely promotes repair of the oxidative damage in the trypanosome's genome.

The amoebozoa are a phylum of protozoans that diverged early in eukaryotic evolution. The amoebozoa include a large number of species that are classified into major subclades. Representative species from these subclades were recently found to have many genes that are related specifically to meiosis and to recombinational repair. This finding suggests that most amoebozoans are likely capable of meiosis, and contributes further to the idea that sex is a primitive character of eukaryotes.

Sexual processes in microbial eukaryotes are often induced by stress. In addition to the examples described above, sexual processes have also been demonstrated to be inducible by stress in other microbial eukaryotes. As an example, when *Chlamydomonas reinhardtii*, a unicellular green alga, is grown in a medium with limiting nitrogen, it differentiates to form gametes that are able to fuse together to produce a zygote capable of meiosis [77]. As another example, when the hyphae of the oomycete *Phytophthora cinnamomi* are exposed to hydrogen peroxide or mechanical damage, sexual reproduction is induced [78]. Also, meiotic processes can be induced in the human fungal pathogen *Cryptococcus neoformans* by desiccation or nitrogen starvation [79].

As noted in Section 1, the main focus of this review is to understand the principal adaptive function of meiotic sexual reproduction in microbial eukaryotes. The evidence reviewed in the preceding sections suggests that meiotic homologous recombination, the central process of meiosis, is an adaption for repairing DNA

**147**

**Author details**

AZ, USA

Harris Bernstein and Carol Bernstein\*

provided the original work is properly cited.

\*Address all correspondence to: bernstein324@yahoo.com

*Sexual Processes in Microbial Eukaryotes DOI: http://dx.doi.org/10.5772/intechopen.88469*

**Conflict of interest**

damages. The need for repair of DNA damages may be particularly critical in response to stress. The alternative possibility, that meiotic sex is primarily an adaptation for generating genetic variation seems less plausible because in well studied microbial eukaryotes, such as *S. cerevisiae* and *S. paradoxus,* all but a small percentage of matings in nature are between clonally related individuals. Nevertheless, the existence of mating types as in *S. cerevisiae, N. crassa* and other microbial eukaryotes suggests that some degree of out-crossing is adaptively beneficial. The benefit of out-crossing is that it promotes complementation, the masking of deleterious recessive mutations in diploid cells [80]. This masking benefit of out-crossing is generally recognized as underlying such concepts as heterosis, hybrid vigor or the avoidance of "inbreeding depression" [81]. Also, sexual processes can produce genetic variation that may be beneficial, as in the case of *C. albicans* populations where parasexual recombination can apparently facilitate, over successive genera-

tions, the evolution of resistance to the antifungal agent fluconazole [38].

Department of Cellular and Molecular Medicine, University of Arizona, Tucson,

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

Both authors declare that they have no conflict of interest.

*Sexual Processes in Microbial Eukaryotes DOI: http://dx.doi.org/10.5772/intechopen.88469*

*Parasitology and Microbiology Research*

invading fungal pathogens.

damage is repaired by homologous recombination.

sex may be a response to oxidative DNA damage.

damage in the trypanosome's genome.

tion or nitrogen starvation [79].

closely genetically related individuals. Thus sex in these species is unlikely to be primarily maintained by an adaptive benefit of producing genetic variation. The ascomycete *S. pombe*, like *S. cerevisiae*, tends to mate when nutrients are scarce. Introduction of DNA damage by different DNA damaging conditions stimulates sexual reproduction and meiotic recombination, consistent with the idea that meiotic recombination is an adaptation for repair. Another ascomycete, *C. albicans* is regarded as a parasexual, rather than sexual, species since it appears to undergo a meiotic process that is not associated with the organized chromosome segregation that normally results in haploid meiotic products. Nevertheless *C. albicans* contains a set of genes homologous to genes that function in meiosis in other species including a key gene that only functions in meiosis. Same sex mating in *C. albicans* likely occurs frequently in nature especially under environmental stress conditions. *U. maydis* is a basidiomycete fungus. Upon infecting its plant host it can undergo meiosis. Recombinational repair occurring during meiosis likely helps protect the *U. maydis* genome from oxidative attack by the plant host's defensive system against

*Paramecium tetraurelia*, a unicellular ciliate, undergoes clonal aging over successive asexual generations leading eventually to extinction. However, if aging paramecia are allowed to undergo a sexual process, either conjugation (mating with another individual) or automixis (self-fertilization), the progeny have a lifespan characteristic of youthful paramecia. During clonal aging DNA damage dramatically increases. Presumably, during automixis or conjugation, age-related DNA

*Volvox carteri* is a facultatively sexual colonial green algae. Sex (syngamy and meiosis) can be induced by conditions that cause oxidative stress, suggesting that

*T. brucei* is a trypanosome parasite that causes human sleeping sickness. The tsetse fly acts as a vector for transmitting the parasite. *T. brucei* after infecting the fly is able to undergo meiosis in the fly's salivary glands. The tsetse fly can defend itself against *T. brucei* infection, in part, by producing DNA damaging reactive oxygen species. When the trypanosomes within the fly's salivary glands undergo meiosis, the associated homologous recombination likely promotes repair of the oxidative

The amoebozoa are a phylum of protozoans that diverged early in eukaryotic evolution. The amoebozoa include a large number of species that are classified into major subclades. Representative species from these subclades were recently found to have many genes that are related specifically to meiosis and to recombinational repair. This finding suggests that most amoebozoans are likely capable of meiosis, and contributes further to the idea that sex is a primitive character of eukaryotes. Sexual processes in microbial eukaryotes are often induced by stress. In addition

to the examples described above, sexual processes have also been demonstrated to be inducible by stress in other microbial eukaryotes. As an example, when *Chlamydomonas reinhardtii*, a unicellular green alga, is grown in a medium with limiting nitrogen, it differentiates to form gametes that are able to fuse together to produce a zygote capable of meiosis [77]. As another example, when the hyphae of the oomycete *Phytophthora cinnamomi* are exposed to hydrogen peroxide or mechanical damage, sexual reproduction is induced [78]. Also, meiotic processes can be induced in the human fungal pathogen *Cryptococcus neoformans* by desicca-

As noted in Section 1, the main focus of this review is to understand the principal adaptive function of meiotic sexual reproduction in microbial eukaryotes. The evidence reviewed in the preceding sections suggests that meiotic homologous recombination, the central process of meiosis, is an adaption for repairing DNA

**146**

damages. The need for repair of DNA damages may be particularly critical in response to stress. The alternative possibility, that meiotic sex is primarily an adaptation for generating genetic variation seems less plausible because in well studied microbial eukaryotes, such as *S. cerevisiae* and *S. paradoxus,* all but a small percentage of matings in nature are between clonally related individuals. Nevertheless, the existence of mating types as in *S. cerevisiae, N. crassa* and other microbial eukaryotes suggests that some degree of out-crossing is adaptively beneficial. The benefit of out-crossing is that it promotes complementation, the masking of deleterious recessive mutations in diploid cells [80]. This masking benefit of out-crossing is generally recognized as underlying such concepts as heterosis, hybrid vigor or the avoidance of "inbreeding depression" [81]. Also, sexual processes can produce genetic variation that may be beneficial, as in the case of *C. albicans* populations where parasexual recombination can apparently facilitate, over successive generations, the evolution of resistance to the antifungal agent fluconazole [38].
