Fungi under Modified Atmosphere—The Effects of CO2 Stress on Cell Membranes and Description of New Yeast Stenotrophomyces fumitolerans gen. nov., sp. nov.
Abstract
:1. Introduction
2. Materials and Methods
2.1. Isolation and Ecology
2.2. Cultivation and Modified Atmosphere Packaging of Strains
2.3. Phylogenetic Analyses
2.4. Fatty Acid Analysis
2.5. Physiology and Chemotaxonomy of Strains WT5 and WR1
3. Results
3.1. Growth Assessment
3.2. Phylogenetic Analyses
3.3. Fatty Acid Compositions
3.4. Taxonomy of Novel Yeast Species
3.5. Description of Stenotrophomyces fumitolerans Gen. Nov., Sp. Nov.
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
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Source | Strain | Species According to NCBI BLAST | Sequence Similarity with Closely-Related Type Strain | Sequence Accession No. |
---|---|---|---|---|
Vegetarian wrap | WR1 | Torulaspora globosa | 96.9% ‡ (KY109865.1) | OQ255941 |
WT2 | Pichia fermentans | 99.8% ‡ (MK394169.1) | OQ255937 | |
WT5 | Vanderwaltozyma verrucispora | 89.0% * (NR_137559.1) | OQ255923 | |
Torulaspora globosa | 96.9% ‡ (KY109865.1) | OQ255942 | ||
Further accession numbers for SSU-ITS-LSU fragment, RPB2 and TEF1 | - | OQ708375, OQ715316, OR661267 | ||
WT6 | Apiotrichum gracile | 99.8% ‡ (KY106124.1) | OQ255938 | |
WT7 | Candida oleophila | 99.6% ‡ (NG_060820.1) | OQ255939 | |
Minced Meat | HR2 | Penicillium griseofulvum | 99.8% * (MH854925.1) | OQ255924 |
Penicillium dipodomyus † | 100% ‡ (MH874450.1) | OQ255931 | ||
HT4 | Candida sake | 100% ‡ (KY106745.1) | OQ255932 | |
Salmon | LR1 | Candida zeylanoides | 100% ‡ (NG_060834.1) | OQ255933 |
LT1 | Didymella corylicola † | 100% ‡ (MN954290.1) | OQ255934 | |
Coffee | KR3 | Neurospora tetraspora | 98.9% ‡ (NG_068996.1) | OQ255940 |
Airborne | TS1 | Penicillium tardochrysogenum † | 100% * (MH865983.1) | OQ255929 |
Penicillium dipodomyus † | 100% ‡ (MH874450.1) | OQ255935 | ||
TS2 | Penicillium griseofulvum | 99.8% * (MH854925.1) | OQ255930 | |
Penicillium tardochrysogenum † | 100% ‡ (NG_070021.1) | OQ255936 | ||
Mofettes | M1 | Rhizopus oryzae | 100% * (DQ641279.1) | OQ255925 |
M2 | Cladosporium subuliforme † | 100% * (MH864124.1) | OQ255922 | |
M3 | Rhodotorula alborubescens | 99.6% * (NR_153197.1) | OQ255926 | |
M4 | Alternaria alstroemeriae † | 100% * (NR_163686.1) | OQ255927 | |
M6 | Penicillium glandicola | 100% * (MH860946.1) | OQ255928 | |
M12 | Rhodotorula babjevae | 99.4% * (NR_077096.1) | OQ504373 | |
International Space Station (ISS) | IF2SW-F4 | Penicillium rubens | 100.0% (MT558923.1) | JACSPE000000000 |
Cantaloupe melon | DSM 1075 | Penicillium rubens | 100% * (NR_111815.1) | PKG00000000, as published before [22] |
Organisms | Growth at | C14:0 | C16:0 | C16:1 cis 9 | C18:0 | C18:1 cis 9 | C18:2 cis 9, 12 | C18:3 cis 9, 12, 15 | C18:1 cis 11 | C18:0 3OH | WAMT (°C) | DU |
---|---|---|---|---|---|---|---|---|---|---|---|---|
Candida zeylanoides LR1 | 10 °C, CO2 | 10.4 ± 0.5 | 8.9 ± 1.8 | <1 | 38.7 ± 3.1 | 24.8 ± 1.9 | 17.3 ± 2.6 | nd | 7.7 ± 0.2 | 1.49 | ||
10 °C | <1 | 11.5 ± 1.5 | 8.4 ± 2.1 | 39.6 ± 3.1 | 25.8 ± 0.5 | 14.7 ± 4.0 | nd | 8.7 ± <0.1 | 1.44 | |||
25 °C | 15.1 ± 0.6 | 4.5 ± 0.3 | 41.3 ± 1.7 | 27.0 ±0.3 | 12.0 ± 1.3 | 11.5 ± 0.1 | 1.36 | |||||
Pichia fermentans WT2 | 10 °C, CO2 | 11.4 ± 1.6 | 19.8 ± 1.7 | 0.5 ± 0.2 | 22.9 ± 2.1 | 22.9 ± 1.3 | 22.4 ± 0.4 | nd | 6.4 ± 0.7 | 1.56 | ||
10 °C | <1 | 11.1 ± 0.9 | 23.1 ± 0.4 | 1.0 ± 0.1 | 24.9 ± 1.2 | 27.1 ± 1.0 | 12.8 ± 0.5 | nd | 7.6 ± 0.5 | 1.41 | ||
25 °C | 14.8 ± 0.4 | 15.7 ± 1.6 | 2.2 ± 0.3 | 21.4 ± 1.3 | 35.6 ± 0.2 | 10.3 ± 0.3 | 9.9 ± 0.6 | 1.39 | ||||
Stenotrophomyces fumitolerans WT5 | 10 °C, CO2 | 5.6 ± 0.7 | 74.2 ± 2.6 | <1 | 16.4 ± 2.0 | nd | nd | 3.8 ± 0.7 | 7.0 ± 0.7 | 0.94 | ||
10 °C | <1 | 8.3 ± 0.3 | 74.5 ± 0.8 | 13.5 ± 0.3 | 3.8 ± 0.7 | nd | 8.4 ± 0.2 | 0.92 | ||||
25 °C | 9.3 ± 1.5 | 65.5 ± 3.3 | 18.2 ± 1.9 | 7.0 ± 1.0 | 10.0 ± 1.0 | 0.91 | ||||||
Stenotrophomyces fumitolerans WR1 | 10 °C, CO2 | 8.6 ± 0.5 | 75.6 ± 0.1 | <1 | 13.1 ± 0.2 | nd | nd | 2.7 ± 0.3 | 8.3 ± 0.3 | 0.91 | ||
10 °C | <1 | 9.0 ± 0.5 | 79.7 ± 4.6 | 9.2 ± 3.5 | 2.9 ± 0.8 | nd | 8.2 ± 0.2 | 0.91 | ||||
25 °C | 10.5 ± 0.4 | 66.4 ± 1.2 | 17.2 ± 1.0 | 5.9 ± 0.4 | 10.4 ± 0.4 | 0.89 | ||||||
Apiotrichum gracile WT6 | 10 °C, CO2 | 16.2 ± 1.0 | 1.4 ± 0.3 | 2.4 ± 2.8 | 19.6 ± 1.0 | 47.2 ± 4.2 | 14.0 ± 1.7 | nd | 8.7 ± 2.3 | 1.57 | ||
10 °C | <1 | 19.1 ± 1.8 | 2.3 ± 0.4 | 2.3 ± 0.4 | 47.5 ± 3.0 | 22.9 ± 3.0 | 5.9 ± 1.4 | nd | 17.2 ± 2.0 | 1.13 | ||
25 °C | 20.8 ± 1.1 | 0.8 ± 0.3 | 3.9 ± 1.2 | 24.0 ± 1.7 | 46.4 ± 2.8 | 4.2 ± 3.9 | 14.9 ± 0.6 | 1.30 | ||||
Candida oleophila WT7 | 10 °C, CO2 | 12.4 ± 0.5 | 12.4 ± 1.1 | 0.3 ± 0.1 | 35.6 ± 0.4 | 19.1 ± 0.9 | 20.1 ± 0.3 | nd | 8.9 ± 0.3 | 1.37 | ||
10 °C | <1 | 14.3 ± 0.5 | 15.7 ± 1.0 | 0.8 ± 0.1 | 41.9 ± 3.8 | 16.8 ± 1.3 | 10.3 ± 2.7 | nd | 12.6 ± 1.1 | 1.22 | ||
25 °C | 14.7 ± 0.4 | 1.8 ± 0.1 | 3.7 ± 0.3 | 47.8 ± 0.7 | 23.7 ± 0.4 | 8.2 ± 0.8 | 15.2 ± 0.6 | 1.22 | ||||
Candida sake HT4 | 10 °C, CO2 | 11.1 ± 0.5 | 11.5 ± 2.7 | 0.7 ± 0.3 | 34.0 ± 8.8 | 28.7 ± 6.8 | 14.0 ± 4.5 | nd | 8.2 ± 0.2 | 1.45 | ||
10 °C | <1 | 14.3 ± 1.2 | 14.7 ± 0.1 | 1.1 ± 0.1 | 50.5 ± 3.4 | 13.7 ± 3.1 | 5.8 ± 1.6 | nd | 14.6 ± 1.6 | 1.10 | ||
25 °C | 12.3 ± 0.7 | 10.5 ± 0.2 | 1.5 ± 0.3 | 48.0 ± 4.6 | 23.0 ± 3.1 | 4.7 ± 1.3 | 12.8 ± 0.8 | 1.19 | ||||
Rhodotorula alborubescens M3 | 10 °C, CO2 | 10.4 ± 0.5 | 0.9 ± 0.1 | 1.9 ± 0.1 | 28.5 ± 0.8 | 39.1 ± 1.1 | 19.2 ± 0.4 | nd | 6.4 ± 0.4 | 1.65 | ||
10 °C | <1 | 20.4 ± 1.3 | 1.4 ± 0.2 | 2.4 ± 0.5 | 46.8 ± 2.3 | 20.9 ± 2.1 | 8.1 ± 1.4 | nd | 17.9 ± 1.5 | 1.14 | ||
25 °C | 18.1 ± 0.5 | 0.4 ± 0.1 | 4.0 ± 0.2 | 54.3 ± 0.8 | 17.6 ± 0.6 | 5.6 ± 0.4 | 19.0 ± 0.3 | 1.06 | ||||
Rhodotorula babjevae M12 | 10 °C, CO2 | 1.0 ± <0.1 | 13.7 ± 0.3 | 2.1 ± 0.2 | 1.4 ± 0.2 | 25.8 ± 0.9 | 25.6 ± 0.2 | 18.9 ± 0.3 | 11.5 ± 0.5 | 19.2 ± 0.4 | 1.70 | |
10 °C | 1.0 ± 0.2 | 16.9 ± 0.9 | 3.2 ± 0.5 | 1.0 ± 0.4 | 36.5 ± 2.8 | 15.5 ± 0.8 | 9.6 ± 2.3 | nd | 16.1 ± 1.3 | 28.7 ± 0.8 | 1.48 | |
25 °C | 1.1 ± 0.1 | 17.7 ± 1.2 | 1.2 ± 0.1 | 1.7 ± 0.2 | 39.0 ± 3.3 | 20.2 ± 2.9 | 10.3 ± 1.9 | 8.5 ± 0.5 | 22.1 ± 1.7 | 1.38 |
Organisms | Growth at | C16:0 | C16:1 cis 9 | C18:0 | C18:1 cis 9 | C18:2 cis 9, 12 | C18:3 cis 9, 12, 15 | WAMT (°C) | DU |
---|---|---|---|---|---|---|---|---|---|
Penicillium rubens IF2SW-F4 | 10 °C, CO2 | 8.8 ± 0.5 | 6.5 ± 1.0 | 11.1 ± 1.7 | 43.7 ± 3.8 | 30.0 ± 4.8 | 4.7 ± 0.2 | 1.89 | |
10 °C | 14.9 ± 0.6 | <1 | 7.2 ± 1.4 | 10.2 ± 1.2 | 51.0 ± 2.7 | 16.7 ± 0.6 | 10.0 ± 1.7 | 1.64 | |
25 °C | 16.1 ± 1.1 | 3.6 ± 0.9 | 8.7 ± 0.5 | 60.0 ± 2.7 | 11.6 ± 1.0 | 8.0 ± 1.3 | 1.63 | ||
Penicillium rubens DSM 1075 | 10 °C, CO2 | 8.9 ± 0.4 | 6.8 ± 2.9 | 4.2 ± 2.2 | 47.3 ± 4.6 | 32.8 ± 4.5 | 3.6 ± 1.4 | 1.97 | |
10 °C | 10.6 ± 1.3 | <1 | 10.1 ± 2.9 | 2.7 ± 0.9 | 44.5 ± 6.2 | 33.0 ± 5.6 | 6.8 ± 1.5 | 1.91 | |
25 °C | 16.0 ± 1.6 | 4.0 ± 0.6 | 3.5 ± 0.5 | 61.5 ± 5.2 | 15.1 ± 3.2 | 7.0 ± 1.6 | 1.72 | ||
Penicillium griseofulvum HR2 | 10 °C, CO2 | 10.5 ± 1.2 | 1.6 ± 0.5 | 2.3 ± 1.1 | 6.9 ± 1.0 | 64.2 ± 3.3 | 14.5 ± 2.3 | 2.7 ± 1.8 | 1.80 |
10 °C | 13.0 ± 0.4 | 1.6 ± 0.3 | 4.2 ± 0.8 | 8.0 ± 0.9 | 55.7 ± 3.3 | 17.5 ± 2.2 | 6.0 ± 0.5 | 1.74 | |
25 °C | 14.8 ± 0.9 | 0.8 ± 0.1 | 2.9 ± 0.3 | 8.0 ± 0.4 | 70.2 ± 2.2 | 3.4 ± 1.1 | 6.8 ± 0.8 | 1.59 | |
Didymella corylicola LT1 | 10 °C, CO2 | 14.8 ± 2.3 | 3.9 ± 0.7 | 1.5 ± 0.2 | 12.9 ± 2.2 | 58.6 ± 2.3 | 8.4 ± 2.6 | 6.8 ± 2.2 | 1.59 |
10 °C | 18.8 ± 1.5 | 8.1 ± 2.2 | 3.0 ± 1.0 | 33.8 ± 3.9 | 33.8 ± 5.0 | 2.5 ± 0.5 | 15.5 ± 2.0 | 1.17 | |
25 °C | 14.4 ± 1.8 | 1.0 ± 0.6 | 2.8 ± 0.1 | 20.7 ± 5.4 | 57.9 ± 6.5 | 3.2 ± 1.5 | 9.1 ± 2.4 | 1.47 | |
Neurospora tetraspora KR3 | 10 °C, CO2 | 10.2 ± 1.8 | 1.5 ± 1.0 | 1.5 ± 0.4 | 5.8 ± 0.6 | 54.3 ±2.4 | 26.8 ± 3.5 | 1.1 ± 1.7 | 1.96 |
10 °C | 12.1 ± 1.3 | 3.2 ± 0.8 | 4.7 ± 1.8 | 15.5 ± 3.2 | 53.2 ± 1.6 | 11.2 ± 1.3 | 7.7 ± 1.6 | 1.59 | |
25 °C | 15.0 ± 1.2 | 1.5 ± 0.1 | 8.0 ± 2.8 | 25.7 ± 3.0 | 45.0 ± 3.1 | 4.8 ± 2.2 | 14.4 ± 2.1 | 1.32 | |
Penicillium tardochrysogenum TS1 | 10 °C, CO2 | 11.0 ± 1.1 | <1 | 4.5 ± 0.4 | 13.4 ± 1.5 | 42.5 ± 4.2 | 28.5 ± 6.5 | 5.4 ± 1.1 | 1.84 |
10 °C | 13.8 ± 0.9 | 5.8 ± 0.9 | 10.7 ± 1.3 | 44.0 ± 2.6 | 25.6 ± 3.3 | 7.9 ± 0.4 | 1.76 | ||
25 °C | 15.0 ± 0.4 | 2.5 ± 0.4 | 23.3 ± 3.0 | 50.4 ± 6.9 | 8.8 ± 3.3 | 9.4 ± 0.9 | 1.50 | ||
Penicillium griseofulvum TS2 | 10 °C, CO2 | 10.3 ± 0.8 | 1.7 ± 0.9 | 2.5 ± 1.1 | 6.2 ± 1.4 | 64.6 ± 4.8 | 14.7 ± 2.3 | 2.6 ± 1.5 | 1.81 |
10 °C | 12.9 ± 0.6 | 1.6 ± 0.4 | 2.6 ± 0.8 | 8.1 ± 0.8 | 60.8 ± 3.5 | 14.0 ± 4.2 | 4.9 ± 0.6 | 1.73 | |
25 °C | 14.6 ± 1.0 | 0.8 ± 0.1 | 3.0 ± 0.6 | 8.6 ± 0.7 | 70.2 ± 3.0 | 2.7 ± 0.9 | 6.9 ± 1.2 | 1.58 | |
Rhizopus oryzae M1 * | 10 °C, CO2 | 25.5 ± 4.4 | 8.0 ± 2.9 | 2.1 ± 0.3 | 35.1 ± 4.1 | 11.6 ± 2.0 | 17.7 ± 4.8 | 19.2 ± 4.0 | 1.19 |
10 °C | 20.3 ± 0.4 | 5.0 ± 1.0 | 6.5 ± 2.5 | 50.4 ± 1.6 | 8.8 ± 2.4 | 9.0 ± 2.0 | 22.0 ± 2.3 | 1.00 | |
25 °C | 22.0 ± 3.5 | 0.9 ± 0.4 | 6.1 ± 1.1 | 42.1 ± 1.5 | 19.4 ± 1.5 | 9.5 ± 1.4 | 20.9 ± 2.8 | 1.10 | |
Cladosporium subuliforme M2 | 10 °C, CO2 | 20.6 ± 2.2 | <1 | 2.4 ± 0.4 | 16.2 ± 0.9 | 49.9 ± 2.1 | 10.9 ± 0.8 | 11.7 ± 1.5 | 1.49 |
10 °C | 22.8 ±1.6 | 5.4 ± 2.8 | 28.2 ± 0.2 | 37.3 ± 0.1 | 6.3 ± 0.8 | 18.1 ± 1.0 | 1.22 | ||
25 °C | 29.1 ± 2.4 | 8.4 ± 1.8 | 33.7 ± 0.8 | 27.9 ± 4.0 | 0.9 ± 0.2 | 26.1 ± 2.7 | 0.92 | ||
Alternaria alstroemeriae M4 | 10 °C, CO2 | 14.6 ± 1.5 | 0.9 ± <0.1 | 5.0 ± 1.0 | 8.3 ± 1.6 | 63.7 ± 1.3 | 7.5 ± 2.0 | 8.2 ± 1.7 | 1.59 |
10 °C | 24.1 ± 1.3 | 1.3 ± <0.1 | 6.2 ± 1.1 | 16.9 ± 0.6 | 47.6 ± 3.2 | 4.0 ± 0.2 | 17.5 ± 1.9 | 1.25 | |
25 °C | 22.3 ± 2.2 | 1.5 ± 0.1 | 6.2 ± 0.6 | 33.9 ± 2.3 | 35.8 ± 0.6 | 0.3 ± <0.1 | 20.0 ± 1.6 | 1.08 | |
Penicillium glandicola M6 | CO2 | 12.0 ± 0.7 | 2.8 ± 0.3 | 2.4 ± 0.4 | 7.7 ± 1.3 | 61.3 ± 2.0 | 13.9 ± 2.7 | 4.1 ± 0.6 | 1.75 |
10 °C | 12.9 ± 0.6 | 1.2 ± 0.1 | 8.3 ± 0.2 | 17.0 ± 1.7 | 50.6 ± 0.9 | 10.0 ± 2.5 | 11.2 ± 0.8 | 1.49 | |
25 °C | 16.4 ± 1.4 | 1.4 ± 0.1 | 6.9 ± 1.4 | 36.7 ± 2.1 | 37.3 ± 1.5 | 1.4 ± 0.5 | 16.9 ± 1.8 | 1.17 |
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Heidler von Heilborn, D.; Reinmüller, J.; Yurkov, A.; Stehle, P.; Moeller, R.; Lipski, A. Fungi under Modified Atmosphere—The Effects of CO2 Stress on Cell Membranes and Description of New Yeast Stenotrophomyces fumitolerans gen. nov., sp. nov. J. Fungi 2023, 9, 1031. https://doi.org/10.3390/jof9101031
Heidler von Heilborn D, Reinmüller J, Yurkov A, Stehle P, Moeller R, Lipski A. Fungi under Modified Atmosphere—The Effects of CO2 Stress on Cell Membranes and Description of New Yeast Stenotrophomyces fumitolerans gen. nov., sp. nov. Journal of Fungi. 2023; 9(10):1031. https://doi.org/10.3390/jof9101031
Chicago/Turabian StyleHeidler von Heilborn, David, Jessica Reinmüller, Andrey Yurkov, Peter Stehle, Ralf Moeller, and André Lipski. 2023. "Fungi under Modified Atmosphere—The Effects of CO2 Stress on Cell Membranes and Description of New Yeast Stenotrophomyces fumitolerans gen. nov., sp. nov." Journal of Fungi 9, no. 10: 1031. https://doi.org/10.3390/jof9101031