Laboratory of Microbial Cultivation and Ecogenomics

Our research focuses on the ecology, evolution, and niche partitioning of freshwater oligotrophs. Small prokaryotes with reduced (streamlined) genomes are the most abundant organisms in the pelagial of freshwater lakes. However, their ecology remains largely elusive because of problems in cultivating environmentally relevant microbes. We apply high-throughput dilution-to-extinction techniques with media mimicking natural conditions and established a large culture collection of typical freshwater genera (>7000 axenic strains, thereof >500 genome-sequenced) from ~100 lakes from five continents spanning all major climatic zones. Our strain collection includes a high diversity of undescribed taxa known only from environmental sequences and a large number of hard-to-grow oligotrophs.

We use a multifaceted approach integrating various methodologies ranging from in situ experiments and field surveys explored by cutting-edge meta-omics to experiments with relevant model organisms. Ecophysiological characterization of cultures and comparative genomics are used to shed light on the ecological niche, (micro)diversity, biogeographic distribution, and evolutionary history of important freshwater lineages. We are further interested in microbial interactions ranging from symbiosis to predation by phages and protists and apply high-throughput techniques to isolate important phages (PhD project of Geyby Carrillo Apolo) and protistan grazers as well as symbiont-host pairs to study their ecological role in freshwater environments.

We currently focus on several ubiquitous freshwater lineages:

  • 'Ca. Patescibacteria' (CPR) - GACR Junior Star project 24-12912M and PhD thesis of Igor Królikiewicz
  • Freshwater SAR11-IIIb ('Ca. Fonsibacter', aka. Allofontibacter, aka. LD12; Alphaproteobacteria) - GACR project 22-03662S and PhD thesis of Clafy Fernandes
  • 'Ca. Nanopelagicales' (aka. acI; Actinomycetota) - GACR project 21-21990S
  • 'Ca. Methylopumilus' (aka. LD28; Gammaproteobacteria) - past GACR project 19-23469S and PhD thesis of Paul Layoun


Lab members

Group leader

Michaela M. Salcher, PhD

Researchers

Markus Haber, PhD

Cecilia Chiriac, PhD

Post-docs

Pawel Markwitz, PhD

Chao-Chin Liu, Ph.D.

PhD students

Paul Layoun, MSc.

Clafy Fernandes, MSc.

Geyby Carrillo Apolo, MSc.

Igor Królikiewicz, MSc.

Laboratory technicians

Alžběta Férová, Mgr.

Ievgen Lebeda, MSc. Ph.D.

Monika Okrouhlíková,MSc. Ph.D.


Former members

Hon Lun (Alan) Wong, PhD now at MPI Bremen, Germany

 



Current projects

High-throughput host detection and cultivation of freshwater CRPs (‘Ca. Patescibacteria’)

Financial support: Czech Science Foundation (GACR); Project No.: 24-12912M, Duration: 2024-2028

Principal Investigator: Cecilia Chiriac

Team Members: Chao-Chin Liu, Igor Królikiewicz, Paul Layoun, Michaela Salcher, Rohit Ghai, Paul Bulzu, Monika Okrouhlíková


Effects of warming and pollutants on nutrient flows and lower trophic levels in freshwater communities: from microbes to Daphnia

 

Financial support: Czech Science Foundation (GACR); Project No.: 24-11779S, Duration: 2024-2026

Principal Investigator: David Boukal, co-PI: Michaela Salcher

Team Members: Tanja Shabarova, Ievgen Lebeda, TBA


Phage host hunt: finding hosts for freshwater phages

Financial support: Czech Science Foundation (GACR); Project No.: 23-06806S, Duration: 2023-2025

Principal Investigator: Markus Haber

Team Members: Pawel Markwitz, Vojtěch Kasalický, Geyby Carrillo Apolo, Ievgen Lebeda, Alžběta Férová


Phylogeography and ecogenomics of 'Ca. Fonsibacter' (SAR11-IIIb)

Financial support: Czech Science Foundation (GACR); Project No.: 22-03662S, Duration: 2022-2024

Principal Investigator: Michaela Salcher

Team Members: Clafy Fernandes, Markus Haber, Cecilia Chiriac, Rohit Ghai, Ievgen Lebeda, Alžběta Férová


EcoFAct – Ecology of abundant freshwater actinobacteria

 

Financial support: Czech Science Foundation (GACR); Project No.: 21-21990S, Duration: 2021-2023

Principal Investigator: Markus Haber

Team Members: Indranil Mukherjee, Michaela Salcher, Rohit Ghai, Karel Šimek, Vinicius Kavagutti, Cecilia Chiriac


Pan-European Lake Sampling - Microbial Eco-genomics (PELAGICS)

Financial support: Czech Science Foundation (GACR); Project No.: 20-12496X, Duration: 2020-2024

Principal Investigator: Rohit Ghai, co-PI: Michaela Salcher

Team Members: Paul Bulzu, Indranil Mukherjee, Alan Wong, Tiberiu Szöke-Nagy, Vojtěch Kasalický, Karel Šimek, Vinicius Kavagutti, Clafy Fernandes, Roudaina Boukheloua, Monika Okrouhlíková, Helena Vieira, Fran Kostanjšek, Petr Macek



Past projects:

Eco-genomics of genome-streamlined freshwater methylotrophs

Financial support: Czech Science Foundation (GACR); Project No.: 19-23469S; Duration: 2019-2021

Principal Investigator: Michaela Salcher

Team Members: Markus Haber, Tanja Shabarova, Paul Bulzu, Paul Layoun, Rohit Ghai, Radka Malá


Eco-genomics of freshwater microbes

Financial support: Money follows Researcher (MFR) grant of the Swiss National Science Foundation (SNSF); Project No.: 310030_185108; Duration: 2019-2020

Principal Investigator: Michaela Salcher

Team Members: Markus Haber




Recent publications (2019-now)

Boukheloua R., Mukherjee I., Park H., Šimek K., Kasalický V., Ngochera M., Grossart H.-P., Picazo-Mozo A., Camacho A., Cabello-Yeves P.J., Rodriguez-Valera F., Callieri C., Andrei A.-S., Pernthaler J., Posch T., Alfreider A., Sommaruga R., Hahn M.W., Sonntag B., Lopez-Garcia P., Moreira D., Jardillier L., Lepère C., Biderre-Petit C., Bednarska A., Ślusarczyk M., Tóth V.R., Banciu H.L., Kormas K., Orlic S., Šantić D., Muyzer G., Herlemann D.P.R., Tammert H., Bertilsson S., Langenheder S., Zechmeister T., Salmaso N., Storelli N., Capelli C., Lepori F., Lanta V., Vieira H.H., Kostanjšek F., Kabeláčová K., Chiriac M.-C., Haber M., Shabarova T., Fernandes C., Rychtecký P., Znachor P., Szőke-Nagy T., Layoun P., Wong H.L., Kavagutti V.S., Bulzu P.-A., Salcher M.M., Piwosz K., Ghai R. (2024) Global freshwater distribution of Telonemia protists. The ISME Journal 18:wrae177. DOI: 10.1093/ismejo/wrae177
Layoun P., López-Pérez M., Haro-Moreno J.M., Haber M., Thrash J.C., Henson M.W., Kavagutti V., Ghai R.Salcher M.M.(2024) Flexible genomic island conservation across freshwater and marine Methylophilaceae. The ISME Journal 18: wrad036. DOI: 10.1093/ismejo/wrad036
Mukherjee I., Grujčić V., Salcher M.M.Znachor P., Seďa J., Devetter M., Rychtecký P.Šimek K.Shabarova T. (2024) Integrating depth-dependent protist dynamics and microbial interactions in spring succession of a freshwater reservoir. Environmental Microbiome 19: 31. DOI: 10.1186/s40793-024-00574-5
Nweze J., Gupta S., Salcher M.M., Šustr V., Horváthová T., Angel R. (2024) Disruption of millipede-gut microbiota in E. pulchripes and G. connexa highlights the limited role of litter fermentation and the importance of litter-associated microbes for nutrition. Communications Biology 7: 1204. DOI: 10.1038/s42003-024-06821-2
Vieira H.H., Bulzu P.-A., Kasalický V., Haber M., Znachor P., Piwosz K., Ghai R., Isolation of a widespread giant virus implicated in cryptophyte bloom collapse, The ISME Journal 18: wrae029. DOI: 10.1093/ismejo/wrae029
Wong H., Bulzu P.-A., Ghai R., Chiriac M.-C., Salcher M.M. (2024) Ubiquitous genome streamlined Acidobacteriota in freshwater environments. ISME Communications 4: ycae124. DOI: 10.1093/ismeco/ycae124
Briddon C.L., Miclăuş M., Hegedüs A., Chiriac M.-C., Nicoară M., Drugă B. (2023) Long-term exposure to elevated temperature leads to altered gene expression in a common bloom-forming cyanobacterium. Limnology and Oceanography 68: 2654–2667. DOI: 10.1002/lno.12448
Fraser M.W., Martin B.C., Wong H., Burns B.P., Kendrick G.A. (2023) Sulfide intrusion in a habitat forming seagrass can be predicted from relative abundance of sulfur cycling genes in sediments. Science of the Total Environment 864: 161144. DOI: 10.1016/j.scitotenv.2022.161144
Bar-Shalom R., Rozenberg A., Lahyani M., Hassanzadeh B., Sahoo G., Haber M., Burgsdorf I., Tang X., Squatrito V., Gómez-Consarnau L., Béjà O., Steindler L. (2023) Rhodopsin-mediated nutrient uptake by cultivated photoheterotrophic Verrucomicrobiota. The ISME Journal 17: 1063–1073. DOI: 10.1038/s41396-023-01412-1

Chiriac M.Haber M., Salcher M.M. (2023) Adaptive genetic traits in pelagic freshwater microbes. Environmental Microbiology 25: 606–641. DOI: 10.1111/1462-2920.16313

Kavagutti V.Bulzu P.Chiriac M., Salcher M.M.Mukherjee I.Shabarova T.,, Grujčić V., Mehrshad M., Kasalický V., Andrei A.S., Jezberová J., Seďa J., Rychtecký P.Znachor P.Šimek K.Ghai R. (2023) High‑resolution metagenomic reconstruction of the freshwater spring bloom. Microbiome 11: 15. DOI: 10.1186/s40168-022-01451-4
Kavagutti V.Chiriac M.Ghai R., Salcher M.M.Haber M. (2023) Isolation of phages infecting the abundant freshwater Actinobacteriota order ‘Ca. Nanopelagicales’. The ISME Journal 17: 943–946. DOI: 10.1038/s41396-023-01400-5
Ngugi D.K., Salcher M.M., Andrei A.S., Ghai R., Klotz F., Chiriac M., Ionescu D., Büsing P., Grossart H., Xing P., Priscu J.C., Alymkulov S., Pester M. (2023) Postglacial adaptations enabled colonization and quasi-clonal dispersal of ammonia-oxidizing archaea in modern European large lakes. Sciences Advances 9: eadc9392. DOI: 10.1126/sciadv.adc9392
Park H.Shabarova T., Salcher M.M., Kosová L., Rychtecký P., Mukherjee I.Šimek K., Porcal P., Seďa J., Znachor P., Kasalický V. (2023) In the right place, at the right time: the integration of bacteria into the Plankton Ecology Group model. Microbiome 11: 112. DOI: 10.1186/s40168-023-01522-0
Šimek K.Mukherjee I.Szöke-Nagy T., Haber M.Salcher M.M.Ghai R. (2023) Cryptic and ubiquitous aplastidic cryptophytes are key freshwater flagellated bacterivores. The ISME Journal 17: 84–94. DOI: 10.1038/s41396-022-01326-4
Briddon C.L., Szekeres E. , Hegedüs A., Nicoară M., Chiriac M., Stockenreiter M., Drugă B. (2022) The combined impact of low temperatures and shifting phosphorus availability on the competitive ability of cyanobacteria. Scientific Reports 12: 16409.
DOI: 10.1038/s41598-022-20580-2
Brad T., Bizic M., Ionescu D., Chiriac M., Kenesz M., Roba C., Ionescu A., Fekete A., Mirea I.C., Moldovan O.T. (2022) Potential for natural attenuation of domestic and agricultural pollution in karst groundwater environments. Water 14: 1597. DOI: 10.3390/w14101597
Chiriac M.Bulzu P., Andrei A.S., Okazaki Y., Nakano S., Haber M.Kavagutti V.Layoun P.Ghai R., Salcher M.M. (2022) Ecogenomics sheds light on diverse lifestyle strategies in freshwater CPR. Microbiome 10: 84. DOI: 10.1186/s40168-022-01274-3
Dirren-Pitsch G., Bühler D., Salcher M.M., Bassin B., Le Moigne A., Schuler M., Pernthaler J., Posch T. (2022) FISHing for ciliates: Catalyzed reporter deposition fluorescence in situ hybridization for the detection of planktonic freshwater ciliates. Frontiers in Microbiology 13: 1070232. DOI: 10.3389/fmicb.2022.1070232
Bulzu P.Kavagutti V., Chiriac M., Vavourakis C.D. , Inoue K. , Kandori H. , Andrei A.S., Ghai R. (2021) Heliorhodopsin evolution is driven by photosensory promiscuity in monoderms. mSphere 6: e00661-21. DOI: 10.1128/mSphere.00661-21
Drugă B., Ramm E., Szekeres E. , Chiriac M., Hegedüs A., Stockenreiter M. (2021) Long-term acclimation might enhance the growth and competitive ability of Microcystis aeruginosa in warm environments. Freshwater Biology 67: 589–602. DOI: 10.1111/fwb.13865
Haber M., Rosenberg D.R., Lalzar M., Burgsdorf I., Saurav K., Lionheart R., Lehahn Y., Aharonovich D., Gómez-Consarnau L., Sher D., Krom M.D., Steindler L. (2022) Spatiotemporal variation of microbial communities in the ultra-oligotrophic Eastern Mediterranean Sea. Frontiers in Microbiology 13: 867694. DOI: 10.3389/fmicb.2022.867694
Johnson M.S., Burns B.P., Herdean A., Angeloski A., Ralph P., Morris T., Kindler G., Wong H., Kuzhiumparambil U., Sedger L.M., Larkum A.W.D. (2022) A cyanobacteria enriched layer of Shark Bay stromatolites reveals a new Acaryochloris strain living in near infrared light. Microorganisms 10: 1035. DOI: 10.3390/microorganisms10051035
Kindler G.S., Wong H., Larkum A.W.D., Johnson M., MacLeod F.I., Burns B.P. (2022) Genome-resolved metagenomics provides insights into the functional complexity of microbial mats in Blue Holes, Shark Bay. FEMS Microbiology Ecology 98: fiab158. DOI: 10.1093/femsec/fiab158
Nobs S.J., MacLeod F.I., Wong H., Burns B.P. (2022) Eukarya the chimera: eukaryotes, a secondary innovation of the two domains of life? Trends in Microbiology 30: 421-431. DOI: 10.1016/j.tim.2021.11.003
Ray A.E., Zaugg J., Benaud N., Chelliah D.S., Bay S., Wong H., Leung P.M., Ji M., Terauds A., Montgomery K., Greening C., Cowan D.A., Kong W., Williams T.J., Hugenholtz P., Ferrari B.C. (2022) Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts. The ISME Journal 16: 2547–2560. DOI: 10.1038/s41396-022-01298-5
Vadaq N., Schirmer M., Tunjungputri R.N., Vlamakis H., Chiriac M., Ardiansyah E., Gasem M.H., Joosten L.A.B., de Groot P.G., Xavier R.J., Netea M.G., van der Ven A., de Mast Q. (2022) Untargeted plasma metabolomics and gut microbiome profiling provide novel insights into the regulation of platelet reactivity in healthy individuals. Thrombosis and Haemostasis 122: 529-539. DOI: 10.1055/a-1541-3706

Haber M., Burgsdorf I., Handley K.M., Rubin-Blum M., Steindler L. (2021) Genomic insights into the lifestyles of Thaumarchaeota inside sponges. Frontiers in Microbiology 11: 622824. DOI: doi.org/10.3389/fmicb.2020.622824

Mujakic I., Andrei A., Shabarova T., Kolesár Fecskeová L., Salcher M.M., Piwosz K., Ghai R., Koblížek M. (2021) Common presence of phototrophic Gemmatimonadota in temperate freshwater lakes. mSystems 6: e01241-20. DOI: 10.1128/mSystems.01241-20
Okazaki Y., Fujinaga S., Salcher M.M., Callieri C., Tanaka A., Kohzu A., Oyagi H., Tamaki H., Nakano S. (2021) Microdiversity and phylogeographic diversification of bacterioplankton in pelagic freshwater systems revealed through long-read amplicon sequencing. Microbiome 9: 24. DOI: 10.1186/s40168-020-00974-y
Piwosz K., Mukherjee I., Salcher M.M., Grujčić V., Šimek K. (2021) CARD-FISH in the sequencing era: Opening a new universe of protistan ecology. Frontiers in Microbiology 12: 640066. DOI: 10.3389/fmicb.2021.640066
Rosenberg D.R., Haber M., Goldford J., Lalzar M., Aharonovich D., Al-Ashhab A., Lehahn Y., Segrè D., Steindler L., Sher D. (2021) Particle-associated and free-living bacterial communities in an oligotrophic sea are affected by different environmental factors. Environmental Microbiology 23: 4295-4308. DOI: 10.1111/1462-2920.15611
Shabarova T., Salcher M.M., Porcal P., Znachor P., Nedoma J., Grossart H., Seďa J., Hejzlar J., Šimek K. (2021) Recovery of freshwater microbial communities after extreme rain events is mediated by cyclic succession. Nature Microbiology 6: 479–488.
DOI: 10.1038/s41564-020-00852-1
Di Cesare A., Dzhembekova N., Cabello-Yeves P.J., Eckert E.M., Slabakova V., Slabakova N., Peneva E., Bertoni R., Corno G., Salcher M.M., Kamburska L., Bertoni F., Rodriguez-Valera F. , Moncheva S., Callieri C. (2020) Genomic comparison and spatial distribution of different Synechococcus phylotypes in the Black Sea. Frontiers in Microbiology 11: 1979. DOI: doi.org/10.3389/fmicb.2020.01979
Kust A., Řeháková K., Vrba J., Maicher V., Mareš J., Hrouzek P., Chiriac M.C., Benedová Z., Tesařová M., Saurav K. (2020) Insight into unprecedented diversity of cyanopeptides in eutrophic ponds using an MS/MS networking approach. Toxins 12: 561. DOI: doi:10.3390/toxins12090561
Mukherjee I., Salcher M.M., Andrei A., Kavagutti V., Shabarova T., Grujčić V., Haber M., Layoun P., Hodoki Y., Nakano S., Šimek K., Ghai R. (2020) A freshwater radiation of diplonemids. Environmental Microbiology 22: 4658–4668. DOI: doi.org/10.1101/2020.05.14.095992
Piwosz K., Shabarova T., Pernthaler J., Posch T., Šimek K., Porcal P., Salcher M.M. (2020) Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. mSphere 5: e00052-20. DOI: 10.1128/mSphere.00052-20

Salcher M.M., Andrei A., Bulzu P., Keresztes Z.G., Banciu H.L., Ghai R. (2020) Visualization of Lokiarchaeia and Heimdallarchaeia (Asgardarchaeota) by fluorescence in situ hybridization and catalyzed reporter deposition (CARD-FISH). mSphere 5: e00686-20. DOI: doi.org/10.1128/mSphere.00686-20

Sizikov S., Burgsdorf I., Handley K.M., Lahyani M., Haber M., Steindler L. (2020), Characterization of sponge‐associated Verrucomicrobia: microcompartment‐based sugar utilization and enhanced toxin–antitoxin modules as features of host‐associated Opitutales. Environmental Microbiology 22: 4669-4688. DOI: https://doi.org/10.1111/1462-2920.15210
Šimek K., Grujčić V., Mukherjee I., Kasalický V., Nedoma J., Posch T., Mehrshad M., Salcher M.M. (2020) Cascading effects in freshwater microbial food webs by predatory Cercozoa, Katablepharidacea and ciliates feeding on aplastidic bacterivorous cryptophytes. FEMS Microbiology Ecology 96: fiaa121. DOI: doi.org/10.1093/femsec/fiaa121
Andrei A., Salcher M.M., Mehrshad M., Rychtecký P.Znachor P.Ghai R. (2019) Niche-directed evolution modulates genome architecture in freshwater Planctomycetes. The ISME Journal 13: 1056–1071. DOI: 10.1038/s41396-018-0332-5
Bulzu P.A., Andrei A., Salcher M.M., Mehrshad M., Inoue K. , Kandori H. , Béjà O., Ghai R., Banciu H.L. (2019) Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche. Nature Microbiology 4: 1129–1137. DOI: 10.1038/s41564-019-0404-y
Callieri C., Slabakova V., Dzhembekova N., Slabakova N., Peneva E., Cabello-Yeves P.J., Di Cesare A., Eckert E.M., Bertoni R., Corno G., Salcher M.M., Kamburska L., Bertoni F., Moncheva S. (2019) The mesopelagic anoxic Black Sea as an unexpected habitat for Synechococcus challenges our understanding of global “deep red fluorescence”. The ISME Journal 13: 1676-1687. DOI: 10.1038/s41396-019-0378-z
Kavagutti V.Andrei A.Mehrshad M., Salcher M.M.Ghai R. (2019) Phage-centric ecological interactions in aquatic ecosystems revealed through ultradeep metagenomics. Microbiome 7: 135. DOI: 10.1186/s40168-019-0752-0
Salcher M.M., Schaefle D., Kaspar M., Neuenschwander S., Ghai R. (2019) Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae. The ISME Journal 13: 2764–2777. DOI: 10.1038/s41396-019-0471-3

CONTACT

Biology Centre CAS
Institute of Hydrobiology
Na Sádkách 702/7
370 05 České Budějovice

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