Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina
Mucoromycotina are often considered mainly in pathogenic context but their biology remains understudied. We describe the genomes of six Mucoromycotina fungi representing distant saprotrophic lineages within the subphylum (i.e., Umbelopsidales and Mucorales). We selected two Umbelopsis isolates from...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-02-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.636986/full |
| _version_ | 1818615519256772608 |
|---|---|
| author | Anna Muszewska Alicja Okrasińska Kamil Steczkiewicz Olga Drgas Małgorzata Orłowska Urszula Perlińska-Lenart Tamara Aleksandrzak-Piekarczyk Katarzyna Szatraj Urszula Zielenkiewicz Sebastian Piłsyk Ewa Malc Piotr Mieczkowski Joanna S. Kruszewska Przemysław Bernat Julia Pawłowska |
| author_facet | Anna Muszewska Alicja Okrasińska Kamil Steczkiewicz Olga Drgas Małgorzata Orłowska Urszula Perlińska-Lenart Tamara Aleksandrzak-Piekarczyk Katarzyna Szatraj Urszula Zielenkiewicz Sebastian Piłsyk Ewa Malc Piotr Mieczkowski Joanna S. Kruszewska Przemysław Bernat Julia Pawłowska |
| author_sort | Anna Muszewska |
| collection | DOAJ |
| description | Mucoromycotina are often considered mainly in pathogenic context but their biology remains understudied. We describe the genomes of six Mucoromycotina fungi representing distant saprotrophic lineages within the subphylum (i.e., Umbelopsidales and Mucorales). We selected two Umbelopsis isolates from soil (i.e., U. isabellina, U. vinacea), two soil-derived Mucor isolates (i.e., M. circinatus, M. plumbeus), and two Mucorales representatives with extended proteolytic activity (i.e., Thamnidium elegans and Mucor saturninus). We complement computational genome annotation with experimental characteristics of their digestive capabilities, cell wall carbohydrate composition, and extensive total lipid profiles. These traits inferred from genome composition, e.g., in terms of identified encoded enzymes, are in accordance with experimental results. Finally, we link the presence of associated bacteria with observed characteristics. Thamnidium elegans genome harbors an additional, complete genome of an associated bacterium classified to Paenibacillus sp. This fungus displays multiple altered traits compared to the remaining isolates, regardless of their evolutionary distance. For instance, it has expanded carbon assimilation capabilities, e.g., efficiently degrades carboxylic acids, and has a higher diacylglycerol:triacylglycerol ratio and skewed phospholipid composition which suggests a more rigid cellular membrane. The bacterium can complement the host enzymatic capabilities, alter the fungal metabolism, cell membrane composition but does not change the composition of the cell wall of the fungus. Comparison of early-diverging Umbelopsidales with evolutionary younger Mucorales points at several subtle differences particularly in their carbon source preferences and encoded carbohydrate repertoire. Nevertheless, all tested Mucoromycotina share features including the ability to produce 18:3 gamma-linoleic acid, use TAG as the storage lipid and have fucose as a cell wall component. |
| first_indexed | 2024-12-16T16:35:12Z |
| format | Article |
| id | doaj.art-102f6f30e3694088baa1c6a8b0612e05 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-16T16:35:12Z |
| publishDate | 2021-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-102f6f30e3694088baa1c6a8b0612e052022-12-21T22:24:29ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-02-011210.3389/fmicb.2021.636986636986Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of MucoromycotinaAnna Muszewska0Alicja Okrasińska1Kamil Steczkiewicz2Olga Drgas3Małgorzata Orłowska4Urszula Perlińska-Lenart5Tamara Aleksandrzak-Piekarczyk6Katarzyna Szatraj7Urszula Zielenkiewicz8Sebastian Piłsyk9Ewa Malc10Piotr Mieczkowski11Joanna S. Kruszewska12Przemysław Bernat13Julia Pawłowska14Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandHigh Throughput Sequencing Facility of UNC, Chapel Hill, NC, United StatesHigh Throughput Sequencing Facility of UNC, Chapel Hill, NC, United StatesInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandDepartment of Industrial Microbiology and Biotechnology, Faculty of Biology and Environmental Protection, University of Łódź, Łódź, PolandInstitute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Warsaw, PolandMucoromycotina are often considered mainly in pathogenic context but their biology remains understudied. We describe the genomes of six Mucoromycotina fungi representing distant saprotrophic lineages within the subphylum (i.e., Umbelopsidales and Mucorales). We selected two Umbelopsis isolates from soil (i.e., U. isabellina, U. vinacea), two soil-derived Mucor isolates (i.e., M. circinatus, M. plumbeus), and two Mucorales representatives with extended proteolytic activity (i.e., Thamnidium elegans and Mucor saturninus). We complement computational genome annotation with experimental characteristics of their digestive capabilities, cell wall carbohydrate composition, and extensive total lipid profiles. These traits inferred from genome composition, e.g., in terms of identified encoded enzymes, are in accordance with experimental results. Finally, we link the presence of associated bacteria with observed characteristics. Thamnidium elegans genome harbors an additional, complete genome of an associated bacterium classified to Paenibacillus sp. This fungus displays multiple altered traits compared to the remaining isolates, regardless of their evolutionary distance. For instance, it has expanded carbon assimilation capabilities, e.g., efficiently degrades carboxylic acids, and has a higher diacylglycerol:triacylglycerol ratio and skewed phospholipid composition which suggests a more rigid cellular membrane. The bacterium can complement the host enzymatic capabilities, alter the fungal metabolism, cell membrane composition but does not change the composition of the cell wall of the fungus. Comparison of early-diverging Umbelopsidales with evolutionary younger Mucorales points at several subtle differences particularly in their carbon source preferences and encoded carbohydrate repertoire. Nevertheless, all tested Mucoromycotina share features including the ability to produce 18:3 gamma-linoleic acid, use TAG as the storage lipid and have fucose as a cell wall component.https://www.frontiersin.org/articles/10.3389/fmicb.2021.636986/fullMucoralesUmbelopsidalesPaenibacilluscomparative genomicscarbon source usagelipid profile |
| spellingShingle | Anna Muszewska Alicja Okrasińska Kamil Steczkiewicz Olga Drgas Małgorzata Orłowska Urszula Perlińska-Lenart Tamara Aleksandrzak-Piekarczyk Katarzyna Szatraj Urszula Zielenkiewicz Sebastian Piłsyk Ewa Malc Piotr Mieczkowski Joanna S. Kruszewska Przemysław Bernat Julia Pawłowska Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina Frontiers in Microbiology Mucorales Umbelopsidales Paenibacillus comparative genomics carbon source usage lipid profile |
| title | Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina |
| title_full | Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina |
| title_fullStr | Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina |
| title_full_unstemmed | Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina |
| title_short | Metabolic Potential, Ecology and Presence of Associated Bacteria Is Reflected in Genomic Diversity of Mucoromycotina |
| title_sort | metabolic potential ecology and presence of associated bacteria is reflected in genomic diversity of mucoromycotina |
| topic | Mucorales Umbelopsidales Paenibacillus comparative genomics carbon source usage lipid profile |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.636986/full |
| work_keys_str_mv | AT annamuszewska metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT alicjaokrasinska metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT kamilsteczkiewicz metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT olgadrgas metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT małgorzataorłowska metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT urszulaperlinskalenart metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT tamaraaleksandrzakpiekarczyk metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT katarzynaszatraj metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT urszulazielenkiewicz metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT sebastianpiłsyk metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT ewamalc metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT piotrmieczkowski metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT joannaskruszewska metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT przemysławbernat metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina AT juliapawłowska metabolicpotentialecologyandpresenceofassociatedbacteriaisreflectedingenomicdiversityofmucoromycotina |