Screening for Volatile α-Unsaturated Ester-Producing Yeasts from the Feces of Wild Animals in South Africa
Abstract
:1. Introduction
2. Materials and Methods
2.1. Biological Materials
2.2. Isolation and Selection of ILV+ Yeast Strains
2.3. Qualitative and Semi-Quantitative Analysis of Volatile Organic Compounds (VOCs)
2.4. Colony PCR and Yeast Identification Using rDNA Sequence Analysis
2.5. Statistical Analysis
3. Results
3.1. Mammalian Feces: An Original Yeast Species Resource
3.2. Selection of ILV+ Strains Producing Volatile Organic Compounds (VOCs)
3.3. VOCs Produced by ILV+ Aroma-Producing Isolates
3.4. Multivariate Analysis of ILV+ Aroma-Producing Yeasts, Isolated Based on Their Origins and Their Volatile Organic Compound Production
3.5. Identification of Strains S12 and S91
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Site Name | Type of Site and Address |
---|---|
Moreleta Kloof Nature Reserve | Game reserve (Helios Street, Moreleta park, Pretoria, Gauteng) |
Kruger National Park | National Park (Kruger National Park, Mpumalanga) |
Lory Park Zoo | Zoo (180/1 Kruger Road, President Park, Midrand, Gauteng) |
McCrindle Farm | Game reserve (Pretoria, Gauteng) |
Emoya big cat sanctuary | Zoo (Farm Milumbe, D1939, Lephalale, Limpopo) |
Elephant Sanctuary | Zoo (Hartbeespoort dam) |
Moholoholo Animal Rehabilitation center | Zoo (Limpopo) |
Animals | Type of Animal | Sampling | Origin | No. of Different Strains |
---|---|---|---|---|
Aardwolf (Proteles cristata) | Carnivorous mammal | Freeze-dried | Not communicated | 2 (S1/S2) |
Abyssinian hornbill (Bucorvus abyssinicus) | Bird | Swab | Lory Park Zoo | 0 |
Bateleur eagle (Terathopius ecaudatus) | Raptor | Swab | Moholoholo Animal Rehabilitation Center | 0 |
Black-and-white-casqued hornbill (Bycanistes subcylindricus) | Bird | Swab | Lory Park Zoo | 1 (S31) |
Black-crested gibbon (Nomascus concolor) | Herbivorous mammal | Swab | Lory Park Zoo | 2 (S3 */S4 *) |
Black jaguar (Panthera pardus) | Carnivorous mammal | Swab | Lory Park Zoo | 3 (S6/S7/S8) |
Black-footed cat (Felis nigripes) | Carnivorous mammal | Tubes | Lory Park Zoo | 4 (S12 */S14/S15/S16)) |
Swab | Lory Park Zoo | 3 (S13 */S17 */S18 *) | ||
Blesbok (Damaliscus pygarus) | Herbivorous mammal | Tube | Moreleta Kloof Nature Reserve | 2 (S9/S10) |
Brown lemur (Eulemur fulvus) | Herbivorous mammal | Swab | Lory Park Zoo | 3 (S58 */S59/S60 *) |
Brown jaguar (Panthera onca) | Carnivorous mammal | Swab | Lory Park Zoo | 5 (S20/S21 */S22 */S23/S24) |
Buffalo (Syncerus caffer) | Herbivorous mammal | Swab | Kruger National Park | 2 (S28 */S29 *) |
Freeze-dried | Not communicated | 1 (S30) | ||
Bushbuck (Tragelaphus sylvaticus) | Herbivorous mammal | Tube | Moreleta Kloof Nature Reserve | 2 (S26/S27 *) |
Swab | Moreleta Kloof Nature Reserve | 0 | ||
Cape vulture (Gyps coprotheres) | Raptor | Swab | Moholoholo Animal Rehabilitation Center | 0 |
Cheetah (Acinonyx jubatus) | Carnivorous mammal | Tube | Lory Park Zoo | 2 (S32/S33 *) |
Swab | Lory Park Zoo | 2 (S34/S35) | ||
Freeze-dried | Not communicated | 0 | ||
Duiker (Sylvicapra grimmia) | Herbivorous mammal | Tube | Moholoholo Animal Rehabilitation Center | 2 (S37 */S38 *) |
Elephant (Loxodonta africana) | Herbivorous mammal | Swab | Kruger National Park | 0 |
Freeze-dried | Not communicated | 1 (S42) | ||
Swab | Elephant Sanctuary | 3 (S39/S40 */S41) | ||
Gibbon (Hylobates lar) | Herbivorous mammal | Swab | Lory Park Zoo | 3 (S43/S44 */S45) |
Giraffe (Giraffa cameopardalis) | Herbivorous mammal | Freeze-dried | Not communicated | 1 (S46) |
Hyena (Crocuta crocuta) | Carnivorous mammal | Swab | Lory Park Zoo | 1 (S47) |
Freeze-dried | Not communicated | 1 (S48) | ||
Impala (Aepyceros melampus) | Herbivorous mammal | Tube | Kruger National Park | 2 (S49/S50) |
Tube | McCrindle Farm | 2 (S51/S52) | ||
King vulture (Sarcoramphus papa) | Raptor | Swab | Lory Park Zoo | 0 |
Kudu (Tragelaphus strepsiceros) | Herbivorous mammal | Tube | McCrindle Farm | 2 (S53/S54) |
Lappet-faced vulture (Torgos tracheliotos) | Raptor | Swab | Moholoholo Animal Rehabilitation Center | 0 |
Lemur (Varecia variegate) | Herbivorous mammal | Tube | Lory Park Zoo | 3 (S55/S56/S57) |
Swab | Lory Park Zoo | 0 | ||
Leopard (Panthera pardus) | Carnivorous mammal | Swab | Lory Park Zoo | 7 (S62 */S63 */S64 */S65 */S68 */S69/S70 *) |
Tube | Lory Park Zoo | 2 (S66/S67) | ||
Freeze-dried | Not communicated | 0 | ||
Lion (Panthera leo) | Carnivorous mammal | Freeze-dried | Not communicated | 1 (S80) |
Tube | Emoya big cat sanctuary | 10 (S71/S72 */S78 */S73/S74 */S75 */S76/S77/S79/S80) | ||
Swab | Emoya big cat sanctuary | 1 (S78) | ||
Long-tailed hornbill (Tropicranus albocristatus) | Raptor | Swab | Lory Park Zoo | 0 |
Meerkat (Suricata suricatta) | Carnivorous mammal | Tube | Lory Park Zoo | 3 (S82 */S83/S84 *) |
Nile crocodile (Crocodylus niloticus) | Reptile | Swab | Lory Park Zoo | 4 (S85/S86/S87/S88 *) |
Ostrich (Struthio camelus) | Bird | Swab | Moreleta Kloof Nature Reserve | 2 (S89/S90) |
Palm nut vulture (Gypohierax angolensis) | Raptor | Swab | Lory Park Zoo | 0 |
Serval (Leptailruus serval) | Carnivorous mammal | Tube | Lory Park Zoo | 3 (S91 */S92 * /S93) |
Swab | Lory Park Zoo | 2 (S94/S95) | ||
Southern hornbill (Bucorvus leadbeateri) | Raptor | Swab | Lory Park Zoo | 0 |
Springbok (Antidorcas marsupialis) | Herbivorous mammal | Tube | Moreleta Kloof Nature Reserve | 6 (S96/S97 */S98/S99 */S100 */S101) |
Tawney eagle (Aquila rapax) | Raptor | Swab | Moholoholo Animal Rehabilitation Center | 2 (S102/S103) |
Tiger (Panthera tigris) | Carnivorous mammal | Tube | Lory Park Zoo | 4 (S104/S105 */S106 */S108/ S109) |
Swab | Lory Park Zoo | 1 (S107) | ||
White-headed vulture (Trigonoceps occipitalis) | Raptor | Swab | Lory Park Zoo | 3 (S114 /S115/S116) |
Swab | Moholoholo Animal Rehabilitation Center | 0 | ||
White lion (Panthero leo) | Carnivorous mammal | Swab | Lory Park Zoo | 2 (S117 */S118) |
White rhino (Ceratotherium simum) | Herbivorous mammal | Freeze-dried | Not communicated | 2 (S119/S120) |
Wild dog (Lycaon pictus) | Carnivorous mammal | Freeze-dried | Not communicated | 1 (S113) |
Wildebeest (Connochaetes gnou) | Herbivorous mammal | Tube | Moreleta Kloof Nature Reserve | 2 (S111/S112) |
Freeze-dried | Not communicated | 1 (S110) | ||
Zebra (Equus zebra) | Herbivorous mammal | Swab | Moreleta Kloof Nature Reserve | 2 (S121 */S122) |
Tube | Moreleta Kloof Nature Reserve | 2 (S123 */S124 *) | ||
Swab | McCrindle Farm | 1 (S125 *) | ||
TOTAL | 119 |
Volatile Compounds | Odor Type (1) | IRRexp (2) | IRRth (3) | Producing Strains |
---|---|---|---|---|
ACIDS | ||||
2-methylbutanoic acid | Over-ripe fruit, cashew, sweet | 856 | 846 | S38 |
3-methylbutanoic acid | Sweet | 837 | 828 | S37; S84; S105 |
Butanoic acid | Rancid | 792 | 780 | S37 |
ALCOHOL | ||||
2-phenylethanol | Flower, honey, rose | 1101 | 1114 | S0; S13; S18; S21; S27; S37; S38; S70; S74; S82; S99; S100; S105; S106 |
ESTERS | ||||
2-methylbutyl 2-methylbutanoate | Fruit, apple, rum, berry | 1110 | 1104 | S0 |
2-methylbutyl 3-methylbutanoate | Apple, cheese, earth | 1112 | 1107 | S0 |
2-methylbutyl butanoate | Fruit, spice, butter | 1057 | 1056 | S0 |
2-methylbutyl propanoate | Sweet, banana, fruit, apple, melon, | 975 | 975 | S0 |
2-methylpropyl 2-methylbutanoate | Sweet, fruit | 1002 | 1004 | S0 |
2-methylpropyl 2-methylpropanoate | Pineapple, grape skin, tropical | 955 (4) | 909 | S0; S91; S106 |
2-methylpropyl 3-methylbutanoate | Fruit, apple, raspberry | 892 | 904 | S0; S12; S13; S18; S68; S75; S99 |
2-methylpropyl butanoate | Sweet, fruit | 959 | 955 | S0 |
2-methylpropyl propanoate | Fruit, green ether, sweet, banana | 869 | 863 | S12 |
2-phenylethyl 2-methylbutanoate | Sweet, fruit, herb, floral | 1494 | 1493 | S0 |
2-phenylethyl 3-methylbutanoate | Apricot, sweet, bitter | 1486 | 1488 | S0; S12; S13; S27; S75 |
2-phenylethyl acetate | Rose, floral, fruit, sweet | 1261 | 1265 | S0 |
3-methylbutyl 2-methylbutanoate | Fruit | 1093 | 1102 | S0; S12; S13; S99 |
3-methylbutyl 2-methylpropanoate | Mixed fruit | 1011 | 1013 | S0; S12; S75 |
3-methylbutyl 3-methylbutanoate | Sweet, apple, fruit | 1099 | 1103 | S12; S13; S18; S75; S99; S105; |
3-methylbutyl acetate | Pear, banana | 872 | 871 | S0; S3; S12; S18; S21; S64; S68; S70; S75; S88; S91; S106 |
3-methylbutyl pentanoate | Ripe apple | 1097 | 1090 | S0; S3; S64 |
3-methylbutyl propanoate | Apricot, pineapple | 968 | 964 | S0; S12; S68; S75; S91; S106 |
Butyl 2-methylbutanoate | Fresh, sweet, fruit | 1039 | 1043 | S0; S12; S91; |
Butyl 2-methylpropanoate | Fruit | 951 | 955 | S0; S12; S64; S68; S91; S106 |
Butyl 3-methylbutanoate | Apple, pear, sweet, pineapple, green | 1043 | 1047 | S0; S12; S106 |
Butyl butanoate | Fresh, sweet, fruit | 995 | 993 | S12; S21; S64; S91; S100; S106 |
Butyl propanoate | Sweet, fruit, rum | 907 | 910 | S12; S64; S75; S91; S106 |
Ethyl 2-methylbutanoate | Fruit, green, apple, flower | 842 | 846 | S0; S3; S12; S18; S21; S68; S75; S91; S99; S105; S106 |
Ethyl 3-methylbutanoate | Fruit, blueberry | 847 | 849 | S0; S3; S12; S13; S18; S21; S64; S68; S75; S91; S99; S105; S106 |
Ethyl butanoate | Fruit, pear, pineapple | 799 | 800 | S0; S3; S12; S21; S37; S38; S64; S68; S70; S75; S84; S88; S91; S100; S105; S106 |
Ethyl hexanoate | Fruit, strawberry, anise | 999 | 996 | S12; S64; S68; S84; S91 |
Ethyl octanoate | Flower, fruit, menthol, anise, sweet | 1196 | 1198 | S0; S91 |
Ethyl pentanoate | Fruit, orange, green | 890 | 898 | S12; S13; S64; S68; S75; S84; S91; S106 |
Octyl 2-methylpropanoate (4) | Cream, wax, fruit, earth, fat | 1349 | 1394 | S0 |
Octyl 2-methylbutanoate | Green, must, fruit | 1432 | 1438 | S0 |
Octyl 3-methylbutanoate | Rose, honey, apple, pineapple | 1436 | 1440 | S0 |
Octyl acetate | Floral, fruit, sweet | 1115 | 1149 | S0 |
Octyl butanoate | Herb, fruit, green | 1391 | 1434 | S0 |
Pentyl butanoate | Apricot, pineapple | 1052 | 1093 | S12; S91 |
Propyl 3-methylbutanoate | Sweet, fruit | 947 | 943 | S0; S12; S91 |
α-UNSATURATED ESTERS | ||||
2-methylpropyl (E)-2-methylbut-2-enoate | Herb, pungent | 1039 | 1034 | S0; S12; S13; S91 |
3-methylbutyl (E)-2-methylbut-2-enoate | Floral | 1190 | 1168 | S0; S12; S91 |
3-methylbutyl (E)-3-methylbut-2-enoate | 1178 | 1184 | S12 | |
Butyl (E)-2-methylbut-2-enoate | Floral, herb, warm, fruit | 1091 | 1068 | S0 |
Ethyl (E)-2-methylbut-2-enoate | Fruit | 938 | 936 | S0; S3; S12; S13; S64; S68; S75; S84 S91; S99; S100; S105; S106 |
Ethyl (E)-3-methylbut-2-enoate | - | 922 | 911 | S0; S3; S12; S13; S64; S68; S75; S84; S91; S99; S105; S106 |
Ethyl (E)-but-2-enoate | Fruit, caramel, pungent | 835 | 833 | S0; S21; S64; S106 |
Ethyl (E)-hex-2-enoate | Fruit, slight, pungent | 1041 | 1025 | S12; S91 |
Propyl (E)-2-methylbut-2-enoate | - | 1039 | 1034 | S0 |
Strains | VOC Tot. | Acids | Alcohols | Esters | α-Esters |
---|---|---|---|---|---|
S0 | 38 | - | 1 | 30 | 7 |
S3 | 7 | - | - | 5 | 2 |
S12 | 27 | - | - | 21 | 6 |
S13 | 10 | - | 1 | 6 | 3 |
S18 | 6 | - | 1 | 5 | - |
S21 | 8 | - | 1 | 6 | 1 |
S27 | 2 | - | 1 | 1 | - |
S37 | 5 | 2 | 1 | 2 | - |
S38 | 4 | 1 | 1 | 2 | - |
S64 | 13 | - | - | 10 | 3 |
S68 | 12 | - | - | 10 | 2 |
S70 | 4 | - | 1 | 3 | - |
S74 | 1 | - | 1 | - | - |
S75 | 14 | - | - | 12 | 2 |
S82 | 1 | - | 1 | - | - |
S84 | 6 | 1 | - | 3 | 2 |
S88 | 3 | - | - | 3 | - |
S91 | 21 | - | - | 16 | 5 |
S99 | 8 | - | 1 | 5 | 2 |
S100 | 5 | - | 1 | 3 | 1 |
S105 | 8 | 1 | 1 | 5 | 1 |
S106 | 16 | - | 1 | 12 | 3 |
Variable | VOC | Ac. | Alc. | Est. | α-Est. | Herb. | Carn. | Rept. | Nat. | Dom. |
---|---|---|---|---|---|---|---|---|---|---|
VOCs | 1 | |||||||||
Ac. | −0.211 | 1 | ||||||||
Alc. | −0.514 | 0.169 | 1 | |||||||
Est. | 0.990 | −0.288 | −0.560 | 1 | ||||||
α-est. | 0.938 | −0.262 | −0.551 | 0.903 | 1 | |||||
Herb. | −0.336 | 0.315 | 0.279 | −0.378 | −0.278 | 1 | ||||
Carn. | 0.410 | −0.256 | −0.139 | 0.423 | 0.361 | −0.894 | 1 | |||
Rept. | −0.194 | −0.101 | −0.285 | −0.134 | −0.209 | −0.141 | −0.316 | 1 | ||
Nat. | −0.228 | −0.185 | 0.320 | −0.244 | −0.139 | 0.645 | −0.577 | −0.091 | 1 | |
Dom. | 0.228 | 0.185 | −0.320 | 0.244 | 0.139 | −0.645 | 0.577 | 0.091 | −1.000 | 1 |
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Tan, M.; Caro, Y.; Lebeau, J.; Shum-Cheong-Sing, A.; François, J.M.; Regnier, T.; Petit, T. Screening for Volatile α-Unsaturated Ester-Producing Yeasts from the Feces of Wild Animals in South Africa. Life 2022, 12, 1999. https://doi.org/10.3390/life12121999
Tan M, Caro Y, Lebeau J, Shum-Cheong-Sing A, François JM, Regnier T, Petit T. Screening for Volatile α-Unsaturated Ester-Producing Yeasts from the Feces of Wild Animals in South Africa. Life. 2022; 12(12):1999. https://doi.org/10.3390/life12121999
Chicago/Turabian StyleTan, Mélissa, Yanis Caro, Juliana Lebeau, Alain Shum-Cheong-Sing, Jean Marie François, Thierry Regnier, and Thomas Petit. 2022. "Screening for Volatile α-Unsaturated Ester-Producing Yeasts from the Feces of Wild Animals in South Africa" Life 12, no. 12: 1999. https://doi.org/10.3390/life12121999