W. T. Starmer

The ecology of yeast flora associated with cactiphilic Drosophila and their host plants in the Sonoran desert

Yeasts were isolated from the rotting stems of 7 species of cereoid cacti and 4 species ofDrosophila which utilize them as host plants. The yeast most common among 132 nonidentical isolates from the cacti and 187 nonidentical isolates from the flies, respectively, were:Pichia membranaefaciens (59 and 126),Candida ingens (22 and 8),Torulopsis sonorensis (16 and 20), andCryptococcus cereanus (11 and 14). Isolates capable of utilizingd-xylose were recovered primarily fromD. pachea andL. schotti. Adult flies were present on the substrates whenP. membranaefaciens was at high concentrations. As the pH of the substrates increased, the percent ofC. ingens cells increased relative to other yeast species. Larvae were detected mainly in alkaline substrates, and since adults did not yieldC. ingens to the extent the substrates did,C. ingens may be important in larval nutrition.Torulopsis sonorensis was recovered mainly fromD. mojavensis and its host plants,M. gummosus andL. thurberi. The concentration ofT. sonorensis in the substrates was negatively correlated with the temperature of the substrate.Cryptococcus cereanus was found in high concentrations in suitable tissues for adult flies but most adults did not yield this species to any extent. The yeast habitat diversities from the substrates had the following order:L. thurberi > C. gigantea > C. gigantea soils ≫ M. gummosus > L. schotti > others. Habitat diversity is discussed in relation to the variation of the physical conditions and chemical composition of the substrates. The yeast habitat diversities from the flies had the orderD. pachea > D. mojavensis ≫ D. nigrospiracula > undescribed Species M. The degree of habitat diversity is possibly a function of the surface feeding behavior of the flies.

Chapter 6 – Yeast Ecology

Publisher Summary nThis chapter reviews the studies of the ecology of yeasts in their natural habitats, and the ways in which yeasts have been used to investigate ecological questions. Yeasts are among the earlier colonizers of nutrient rich substrates, where they are followed by a succession of organisms that degrade dead organic matter. However, yeasts are not just decomposers but can assume a diversity of forms and functions in the natural world. Along with their role in the transformation of nutrients, they can engage in intimate relationships with other organisms as mutualists, competitors, parasites, or pathogens. They occur together in communities or guilds linked together through intricate interrelationships. Yeasts are widely distributed throughout all biomes of the world. They have been found in the upper levels of the atmosphere (above the clouds in the stratosphere), in the deepest parts of the oceans, in aquifers under the sea, in ancient glacial ice, and are abundant throughout the phyllosphere. Associates of yeasts include viruses, bacteria, other fungi, algae, vascular plants, and animals of almost any sort.

Relevance of the ecology ofCitrus yeasts to the diet ofDrosophila

A study of the yeast flora of necrotic oranges and associatedDrosophila yielded a total of 221 isolates composed ofKloeckera apiculata (75),Pichia fermentans (75),Pichia kluyveri (50),Torulopsis stellata (17),Hanseniaspora uvarum (2),P. membranaefaciens (1), andCandida vini (1). The yeast species of all samples of oranges and adultDrosophila were very similar; however, the speciesof Drosophila contained a higher proportion ofP. fermentans and a lower proportion ofK. apiculata than was found in the rotting oranges.P. fermentans was subsequently found more frequently on the surface of the necrotic tissue, where the flies feed, than was found internally. SinceP. fermentans characteristically produces a pellicle and pseudomycelium andK. apiculata does not, it is concluded that the growth characteristics of the yeasts are an important factor determining adultDrosophila diets.

Pichia opuntiae, a New Heterothallic Species of Yeast Found in Decaying Cladodes of Opuntia inermis and in Necrotic Tissue of Cereoid Cacti

A new heterothallic species of Pichia has been recovered 25 times from widely separated cactus substrates. The organism has been named Pichia opuntiae because the sexually most compatible strains were isolated from Opuntia inermis in Australia. Two varieties are designated based on differences in physiology, habitat, and geographic distribution. P. opuntiae var. opuntiae has a maximum temperature for growth of 30 to 33°C and assimilates citric acid strongly, but assimilation of cellobiose is latent, weak, or negative. P. opuntiae var. thermotolerans grows well at 37°C, but not at 39°C; it assimilates cellobiose strongly but does not assimilate citric acid. Ecologically, P. opuntiae var. opuntiae is associated with Opuntia inermis (tribe Opuntiaeae, subtribe Opuntiinae) in Australia; P. opuntiae var. thermotolerans is associated with species of the cactus tribe Pachycereeae, subtribe Pachycereinae, from various locations in the North American Sonoran Desert. A discussion of the physiological and host-plant shifts for these two varieties and three similar cactophilic yeasts is presented. The base composition of the nuclear deoxyribonucleic acid of P. opuntiae var. opuntiae (average of four strains) is 33.64 ± 0.25 mol% guanine plus cytosine and that of P. opuntiae var. thermotolerans (average of 3 strains) is 33.13 ± 0.23 mol% guanine plus cytosine. The type strain of P. opuntiae and of the type variety, P. opuntiae var. opuntiae, is UCD-FS&T 77-40 (= ATCC 36836 = CBS 7010). The type strain of P. opuntiae var. thermotolerans is UCD-FS&T 76-211 (= ATCC 36834 = CBS 7012).

Pichia amethionina, a New Heterothallic Yeast Associated with the Decaying Stems of Cereoid Cacti

A new species of the genus Pichia has been recovered 38 times in the Sonoran Desert from “rot pockets” of cereoid cacti and from Drosophila species which utilize the cacti. We have named the species Pichia amethionina due to its absolute requirement for methionine or cysteine. P. amethionina is heterothallic and demonstrates an agglutination reaction when opposite mating types are mixed. Two varieties are designated based on the combination of mannitol assimilation and ecological habitat. P. amethionina var. amethionina, the type variety, was recovered from cacti in the subtribe Stenocereinae and cannot assimilate mannitol, whereas P. amethionina var. pachycereana was found in cacti of the subtribe Pachycereinae and can assimilate mannitol. Results are given which demonstrate that the assimilation of mannitol is controlled by a single genetic locus. An evaluation of the interfertility and postmating viability among the two varieties and possibly identical organisms was made. The base composition of the nuclear deoxyribonucleic acid (average of 10 strains) is 33.05 ± 0.19 mol% guanine plus cytosine. The type strain of P. amethionina and of the type variety, P. amethionina var. amethionina, is UCD-FST 76-401B (=ATCC 36080 = CBS 6940). The type strain of P. amethionina var. pachycereana is UCD-FST 76-384A (=ATCC 36079 = CBS 6943).

Pichia cactophila, a New Species of Yeast Found in Decaying Tissue of Cacti

A novel representative of the yeast genus Pichia has been recovered 190 times during the period 1971 to 1976. We regard this organism as belonging to a new species, Pichia cactophila. Strains were found in the necrotic tissue of 16 species of cactus and in the crops of 3 species of Drosophila which utilize the cacti as host plants. Isolates were obtained from widely separate geographic localities (throughout Mexico, Southwestern United States, and Hawaii). The new species forms predominantly two-spored asci. Both homothallic and heterothallic strains were observed. The metabolic capability of P. cactophila, like that of P. membranaefaciens, is limited to oxidative utilization of only a few compounds. P. cactophila can be differentiated from P. membranaefaciens by its strong growth on D-glucosamine and by the lower guanine-plus-cytosine content (36.3 to 37.5 mol%) of its nuclear deoxyribonucleic acid. The type strain of P. cactophila is UCD-FST 76-243A (= ATCC 34932 = CBS 6926).

Pichia heedii, a New Species of Yeast Indigenous to Necrotic Cacti in the North American Sonoran Desert

A novel member of the yeast genus Pichia was recovered 67 times during the period 1971 to 1976. We have named this new species Pichia heedii in honor of William B. Heed. Most strains were isolated from the soft-rot of Lophocereus schottii and from Drosophila pachea, which utilizes L. schottii as a host plant. All strains were found in the Sonoran Desert. The species has four-spored asci and is heterothallic. P. heedii has metabolic capabilities similar to those of P. membranaefaciens, but the base composition of its nuclear deoxyribonucleic acid is 10 to 12 mol% lower than that of P. membranaefaciens. P. heedii may be differentiated from other cactus-specific Pichia species by its ability to assimilate D-xylose and from P. membranaefaciens by its cactus habitat, small cell size, and relatively high maximum temperature of growth. The type strain of P. heedii is UCD-FST 76-356 (= ATCC 34936 = CBS 6930).

Torulopsis sonorensis, a New Species of the Genus Torulopsis

A novel member of the yeast genus Torulopsis has been recovered 35 times during 1971, 1972, 1973, and 1974 from Drosophila mojavensis, from soft-rot pockets from six species of cacti, and from soil wetted by soft-rot fluid. The collections were made in the Sonoran desert of southern Arizona and of northern Mexico. The new species was named Torulopsis sonorensis after the geography of its habitat. The type strain is UCD (FS&T) 71–148 (= ATCC 32108 = CBS 6792).

Pichia mexicana, a New Heterothallic Yeast from Cereoid Cacti in the North American Sonoran Desert

A description is given of a novel member of the yeast genus Pichia that was recovered 13 times in the Sonoran Desert from necrotic tissue of cereoid cacti. Most of the isolates came from organ-pipe cacti. The new yeast occurs in the cactus “rot pockets” in the haploid condition and is heterothallic. Upon mixing of appropriate mating types, zygotes developed with hat-shaped ascospores. Physiologically, the haploid strains resemble Candida tenuis, but this species has a different habitat and shares only 9.2% of its nuclear deoxyribonucleic acid base sequences with P. mexicana. The sexual state is physiologically similar to P. stipitis and an as yet undescribed cactus-specific species of the genus Clavispora, but their deoxyribonucleic acid sequence complementarity is less than 7% compared with P. mexicana. The base composition of the nuclear deoxyribonucleic acid of P. mexicana ranged from 42.2 to 43.0 mol% guanine plus cytosine (five strains). The type strain of P. mexicana is UCD-FST 76-308A (= ATCC 42175 = CBS 7066) and the complementary mating type is UCD-FST 76-391B (= ATCC 42176 = CBS 7067).

Original Papers Relating to the Systematics of Yeasts: Cryptococcus cereanus, a New Species of the Genus Cryptococcus

A novel representative of the yeast genus Cryptococcus has been recovered 11 times during 1971, 1972, and 1973 from soft-rot pockets in three species of cactus. Cereus schottii Engelm., Cereus giganteus Engelm., and Cereus thurberi Engelm. The collections were made in the Sonoran desert of southern Arizona and of northern Mexico. The rot pockets constitute important breeding sites for Drosophila spp., which presumably feed on the yeasts present. The new species was named after the genus of cactus with which it is associated.