A fungi hotspot deep in the ocean: explaining the presence of Gjaerumia minor in equatorial Pacific bathypelagic waters.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
08 May 2024
08 May 2024
Historique:
received:
14
11
2023
accepted:
06
05
2024
medline:
9
5
2024
pubmed:
9
5
2024
entrez:
8
5
2024
Statut:
epublish
Résumé
A plant parasite associated with the white haze disease in apples, the Basidiomycota Gjaerumia minor, has been found in most samples of the global bathypelagic ocean. An analysis of environmental 18S rDNA sequences on 12 vertical profiles of the Malaspina 2010 expedition shows that the relative abundance of this cultured species increases with depth while its distribution is remarkably different between the deep waters of the Pacific and Atlantic oceans, being present in higher concentrations in the former. This is evident from sequence analysis and a microscopic survey with a species-specific newly designed TSA-FISH probe. Several hints point to the hypothesis that G. minor is transported to the deep ocean attached to particles, and the absence of G. minor in bathypelagic Atlantic waters could then be explained by the absence of this organism in surface waters of the equatorial Atlantic. The good correlation of G. minor biomass with Apparent Oxygen Utilization, recalcitrant carbon and free-living prokaryotic biomass in South Pacific waters, together with the identification of the observed cells as yeasts and not as resting spores (teliospores), point to the possibility that once arrived at deep layers this species keeps on growing and thriving.
Identifiants
pubmed: 38719921
doi: 10.1038/s41598-024-61422-7
pii: 10.1038/s41598-024-61422-7
doi:
Substances chimiques
RNA, Ribosomal, 18S
0
DNA, Ribosomal
0
DNA, Fungal
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
10601Subventions
Organisme : Ministry of Economy and Competitiveness | Agencia Estatal de Investigación de España (Agencia Estatal de Investigación de España)
ID : CSD2008–00077
Organisme : Ministry of Economy and Competitiveness | Agência de Investigação Estadual (Agencia Estatal de Investigación de España)
ID : CTM2016-75083-R
Organisme : Ministry of Economy and Competitiveness | Agência de Investigação Estadual (Agencia Estatal de Investigación de España)
ID : PID2019-105775RB-I00
Informations de copyright
© 2024. The Author(s).
Références
Hansell, D. A., Carlson, C. A., Repeta, D. J. & Schlitzer, R. Dissolved organic matter in the ocean, a controversy stimulates new insights. Oceanography 22, 202–211 (2009).
doi: 10.5670/oceanog.2009.109
Gómez-Letona, M. et al. Deep ocean prokaryotes and fluorescent dissolved organic matter reflect the history of the water masses across the Atlantic Ocean. Prog. Oceanogr. 205, 102819 (2022).
doi: 10.1016/j.pocean.2022.102819
Baltar, F. et al. What is refractory organic matter in the ocean?. Front. Mar. Sci. 8, 1–7 (2021).
doi: 10.3389/fmars.2021.642637
Li, W., Wang, M., Burgaud, G., Yu, H. & Cai, L. Fungal community composition and potential depth-related driving factors impacting distribution pattern and trophic modes from epi- to abyssopelagic zones of the Western Pacific Ocean. Microb. Ecol. 78, 820–831 (2019).
pubmed: 30993370
doi: 10.1007/s00248-019-01374-y
Morales, S. E., Biswas, A., Herndl, G. J. & Baltar, F. Global structuring of phylogenetic and functional diversity of pelagic fungi by depth and temperature. Front. Mar. Sci. 6, 131 (2019).
doi: 10.3389/fmars.2019.00131
Richards, T. A. et al. Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proc. R. Soc. B Biol. Sci. 282, 20152243 (2015).
doi: 10.1098/rspb.2015.2243
Baltar, F., Zhao, Z. & Herndl, G. J. Potential and expression of carbohydrate utilization by marine fungi in the global ocean. Microbiome 9, 106 (2021).
pubmed: 33975640
pmcid: 8114511
doi: 10.1186/s40168-021-01063-4
Breyer, E. & Baltar, F. The largely neglected ecological role of oceanic pelagic fungi. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2023.05.002 (2023).
doi: 10.1016/j.tree.2023.05.002
pubmed: 37246083
Bochdansky, A. B., Clouse, M. A. & Herndl, G. J. Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J. 11, 362–373 (2017).
pubmed: 27648811
doi: 10.1038/ismej.2016.113
Zhang, X. Y. et al. Diversity and antimicrobial activity of culturable fungi isolated from six species of the South China sea gorgonians. Microb. Ecol. 64, 617–627 (2012).
pubmed: 22526402
doi: 10.1007/s00248-012-0050-x
Yue, Y. et al. Exploring the antibacterial and antifungal potential of jellyfish-associated marine fungi by cultivation-dependent approaches. PLoS One 10, e0144394 (2015).
pubmed: 26637162
pmcid: 4670088
doi: 10.1371/journal.pone.0144394
Duarte, A. W. F. et al. Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Environ. Microbiol. Rep. 8, 874–885 (2016).
pubmed: 27518570
doi: 10.1111/1758-2229.12452
Taylor, J. D. & Cunliffe, M. Multi-year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J. 10, 2118–2128 (2016).
pubmed: 26943623
pmcid: 4989315
doi: 10.1038/ismej.2016.24
Jeffries, T. C. et al. Partitioning of fungal assemblages across different marine habitats. Environ. Microbiol. Rep. 8, 235–238 (2016).
pubmed: 26742806
doi: 10.1111/1758-2229.12373
Tisthammer, K. H., Cobian, G. M. & Amend, A. S. Global biogeography of marine fungi is shaped by the environment. Fungal Ecol. 19, 39–46 (2016).
doi: 10.1016/j.funeco.2015.09.003
Pernice, M. C. et al. Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans. ISME J. 10, 945–958 (2016).
pubmed: 26451501
doi: 10.1038/ismej.2015.170
Wang, Q. M. et al. Multigene phylogeny and taxonomic revision of yeasts and related fungi in the Ustilaginomycotina. Stud. Mycol. 81, 55–83 (2015).
pubmed: 26955198
pmcid: 4777779
doi: 10.1016/j.simyco.2015.10.004
Richter, C., Yurkov, A. M., Boekhout, T. & Stadler, M. Diversity of Tilletiopsis-like fungi in Exobasidiomycetes (Ustilaginomycotina) and description of six novel species. Front. Microbiol. 10, 462920 (2019).
doi: 10.3389/fmicb.2019.02544
Boekhout, T. et al. Extensive colonization of apples by smut anamorphs causes a new postharvest disorder. FEMS Yeast Res. 6, 63–76 (2006).
pubmed: 16423072
doi: 10.1111/j.1567-1364.2005.00002.x
Ramani, R., Kahn, B. T. & Chaturvedi, V. Tilletiopsis minor: A new etiologic agent of human subcutaneous mycosis in an immunocompromised host. J. Clin. Microbiol. 35, 2992–2995 (1997).
pubmed: 9350777
pmcid: 230105
doi: 10.1128/jcm.35.11.2992-2995.1997
Al-Zaydani, I. A., Joseph, M. R. P., Suheel, A. M., Al-Hakami, A. M. & Hamid, M. E. Severe pneumonia with a massive pleural effusion in a child caused by Tilletiopsis minor: The first case from Saudi Arabia. Ann. Saudi Med. 35, 475–478 (2015).
pubmed: 26657234
pmcid: 6074469
doi: 10.5144/0256-4947.2015.475
Kechkekian, A., Gari-Toussaint, M., Gastaud, P., Freton, A. & Gantier, J. C. Kératite à Tilletiopsis minor post LASIK. J. Mycol. Med. 17, 119–121 (2007).
doi: 10.1016/j.mycmed.2007.03.001
El Baidouri, F., Zalar, P., James, T. Y., Gladfelter, A. S. & Amend, A. S. Evolution and physiology of amphibious yeasts. Annu. Rev. Microbiol. 75, 337–357. https://doi.org/10.1146/annurev-micro-051421 (2021).
doi: 10.1146/annurev-micro-051421
pubmed: 34351793
Sharon, A. & Shlezinger, N. Fungi infecting plants and animals: Killers, non-killers, and cell death. PLoS Pathog. 9, e1003517 (2013).
pubmed: 24009499
pmcid: 3757032
doi: 10.1371/journal.ppat.1003517
Dickman, M. B. & de Figueiredo, P. Comparative pathobiology of fungal pathogens of plants and animals. PLoS Pathog. 7, e1002324 (2011).
pubmed: 22194681
pmcid: 3240592
doi: 10.1371/journal.ppat.1002324
Kim, J. S., Yoon, S. J., Park, Y. J., Kim, S. Y. & Ryu, C. M. Crossing the kingdom border: Human diseases caused by plant pathogens. Environ. Microbiol. 22, 2485–2495. https://doi.org/10.1111/1462-2920.15028 (2020).
doi: 10.1111/1462-2920.15028
pubmed: 32307848
Köhler, J. R., Hube, B., Puccia, R., Casadevall, A. & Perfect, J. R. Fungi that infect humans. Microbiol. Spectr. 5, 10–1128 (2017).
doi: 10.1128/microbiolspec.FUNK-0014-2016
Giner, C. R. et al. Marked changes in diversity and relative activity of picoeukaryotes with depth in the world ocean. ISME J. 14, 437–449 (2020).
pubmed: 31645670
doi: 10.1038/s41396-019-0506-9
Obiol, A., Muhovic, I. & Massana, R. Oceanic heterotrophic flagellates are dominated by a few widespread taxa. Limnol. Oceanogr. 66, 4240–4253 (2021).
doi: 10.1002/lno.11956
Pernice, M. C. et al. Global abundance of planktonic heterotrophic protists in the deep ocean. ISME J. 9, 782–792 (2015).
pubmed: 25290506
doi: 10.1038/ismej.2014.168
Logares, R. et al. Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome 8, 1–17 (2020).
doi: 10.1186/s40168-020-00827-8
Junger, P. C. et al. Global biogeography of the smallest plankton across ocean depths. Sci. Adv. 9, 9763 (2023).
doi: 10.1126/sciadv.adg9763
Stoeck, T. et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19, 21–31 (2010).
pubmed: 20331767
doi: 10.1111/j.1365-294X.2009.04480.x
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Catalá, T. S. et al. Drivers of fluorescent dissolved organic matter in the global epipelagic ocean. Limnol. Oceanogr. 61, 1101–1119 (2016).
doi: 10.1002/lno.10281
Catalá, T. S. et al. Water mass age and aging driving chromophoric dissolved organic matter in the dark global ocean. Glob. Biogeochem. Cycles 29, 917–934 (2015).
doi: 10.1002/2014GB005048
Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002).
pubmed: 12039771
pmcid: 123953
doi: 10.1128/AEM.68.6.3094-3101.2002
Priest, T., Fuchs, B., Amann, R. & Reich, M. Diversity and biomass dynamics of unicellular marine fungi during a spring phytoplankton bloom. Environ. Microbiol. 23, 448–463 (2021).
pubmed: 33201558
doi: 10.1111/1462-2920.15331
Hillebrand, H., Dürselen, C.-D., Kirschtel, D., Pollingher, U. & Zohary, T. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35, 403–424 (1999).
doi: 10.1046/j.1529-8817.1999.3520403.x
Menden-Deuer, S. & Lessard, E. J. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45, 569–579 (2000).
doi: 10.4319/lo.2000.45.3.0569
Bauer, R., Begerow, D., Nagler, A. & Oberwinkler, F. The Georgefischeriales. Micol. Res. 105, 416–424 (2001).
doi: 10.1017/S0953756201003690
Sánchez, P. et al. Marine picoplankton metagenomes and MAGs from eleven vertical profiles obtained by the Malaspina Expedition. Sci. Data 11, 154 (2024).
pubmed: 38302528
pmcid: 10834958
doi: 10.1038/s41597-024-02974-1
Catalá, T. S. et al. Dissolved organic matter (DOM) in the open Mediterranean sea. I. Basin–wide distribution and drivers of chromophoric DOM. Prog. Oceanogr. 165, 35–51 (2018).
doi: 10.1016/j.pocean.2018.05.002
Coble, P. G. Characterization of marine and terrestrial DOM in seawater using excitation–emission matrix spectroscopy. Mar. Chem. 51, 325–346 (1996).
doi: 10.1016/0304-4203(95)00062-3
Stedmon, C. A. & Markager, S. Resolving the variability in dissolved organic matter fluorescence in a temperate estuary and its catchment using PARAFAC analysis. Limnol. Oceanogr. 50, 686–697 (2005).
doi: 10.4319/lo.2005.50.2.0686
Yamashita, Y. & Tanoue, E. Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids. Mar. Chem. 82, 255–271 (2003).
doi: 10.1016/S0304-4203(03)00073-2
Fellman, J. B., D’Amore, D. V., Hood, E. & Boone, R. D. Fluorescence characteristics and biodegradability of dissolved organic matter in forest and wetland soils from coastal temperate watersheds in southeast Alaska. Biogeochemistry 88, 169–184 (2008).
doi: 10.1007/s10533-008-9203-x
Begerow, D., Stoll, M. & Bauer, R. A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98, 906–916 (2006).
pubmed: 17486967
doi: 10.1080/15572536.2006.11832620
Bauer, R., Lutz, M. & Oberwinkler, F. Gjaerumia, a new genus in the Georgefischeriales (Ustilaginomycetes). Mycol. Res. 109, 1250–1258 (2005).
pubmed: 16279418
doi: 10.1017/S0953756205003783
Boekhout, T. & Washingtonensis Nyland, T. Tilletiopsis Derx ex Derx (1930) Type species (2011).
de Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015).
pubmed: 25999516
doi: 10.1126/science.1261605
Mestre, M. et al. Sinking particles promote vertical connectivity in the ocean microbiome. Proc. Natl. Acad. Sci. U. S. A. 115, E6799–E6807 (2018).
pubmed: 29967136
pmcid: 6055141
doi: 10.1073/pnas.1802470115
Ruiz-González, C. et al. Major imprint of surface plankton on deep ocean prokaryotic structure and activity. Mol. Ecol. 29, 1820–1838 (2020).
pubmed: 32323882
doi: 10.1111/mec.15454
Deng, Y., Wang, K., Hu, Z., Hu, Q. & Tang, Y. Different geographic strains of dinoflagellate Karlodinium veneficum host highly diverse fungal community and potentially serve as possible niche for colonization of fungal endophytes. Int. J. Mol. Sci. 24, 1672 (2023).
pubmed: 36675187
pmcid: 9865425
doi: 10.3390/ijms24021672
Sun, J. Y. et al. Fungal community dynamics during a marine dinoflagellate (Noctiluca scintillans) bloom. Mar. Environ. Res. 131, 183–194 (2017).
pubmed: 29017729
doi: 10.1016/j.marenvres.2017.10.002
Agusti, S. et al. Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump. Nat. Commun. 6, 7608 (2015).
pubmed: 26158221
doi: 10.1038/ncomms8608
Kiko, R. et al. Biological and physical influences on marine snowfall at the equator. Nat. Geosci. 10, 852–858 (2017).
doi: 10.1038/ngeo3042
Clipson, N., Otte, M. & Landy, E. Biogeochemical roles of fungi in marine and estuarine habitats. In Fungi in Biogeochemical Cycles (ed. Pernice, M.) 436–461 (Cambridge University Press, Cambridge, 2006).
doi: 10.1017/CBO9780511550522.019
Frey-Klett, P. et al. Bacterial-fungal interactions: Hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol. Biol. Rev. 75, 583–609 (2011).
pubmed: 22126995
pmcid: 3232736
doi: 10.1128/MMBR.00020-11
Simonato, F. et al. Piezophilic adaptation: A genomic point of view. J. Biotechnol. 126, 11–25. https://doi.org/10.1016/j.jbiotec.2006.03.038 (2006).
doi: 10.1016/j.jbiotec.2006.03.038
pubmed: 16780980
Bass, D. et al. Yeast forms dominate fungal diversity in the deep oceans. Proc. R. Soc. B Biol. Sci. 274, 3069–3077 (2007).
doi: 10.1098/rspb.2007.1067
Sala, M. M. et al. Prokaryotic capability to use organic substrates across the global tropical and subtropical ocean. Front. Microbiol. 11, 528409 (2020).
doi: 10.3389/fmicb.2020.00918
Albu, S., Toome, M. & Aime, M. C. Violaceomyces palustris gen. et sp. Nov. and a new monotypic lineage, Violaceomycetales ord. nov. in Ustilaginomycetes. Mycologia 107, 1193–1204 (2015).
pubmed: 26297779
doi: 10.3852/14-260
Zhou, J., Jiang, W., Ding, J., Zhang, X. & Gao, S. Effect of Tween 80 and β-cyclodextrin on degradation of decabromodiphenyl ether (BDE-209) by White Rot Fungi. Chemosphere 70, 172–177 (2007).
pubmed: 17707457
doi: 10.1016/j.chemosphere.2007.06.036
Martinez, D. et al. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat. Biotechnol. 22, 695–700 (2004).
pubmed: 15122302
doi: 10.1038/nbt967
Márquez-Rocha, F. J., Hernández-Rodríguez, V. Z. & Vázquez-Duhalt, R. Biodegradation of soil-adsorbed polycyclic aromatic hydrocarbons by the white rot fungus Pleurotus ostreatus. Biotechnol. Lett. 22, 469–472 (2000).
doi: 10.1023/A:1005663419547
Mestre, M. & Höfer, J. The microbial conveyor belt: Connecting the globe through dispersion and dormancy. Trends Microbiol. 29, 482–492. https://doi.org/10.1016/j.tim.2020.10.007 (2021).
doi: 10.1016/j.tim.2020.10.007
pubmed: 33281016