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Ecophysiology and global dispersal of the freshwater SAR11-IIIb genus Fontibacterium

Nature Microbiology volume 10, pages 2194–2206 (2025)Cite this article

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Abstract

The SAR11-IIIb genus Fontibacterium within the order ‘Ca. Pelagibacterales’ is recognized for its ubiquitous presence in freshwater environments. However, cultivation limitations have hampered deeper ecophysiological understanding of this genus, with most data limited to lakes in the Northern Hemisphere. Here we present seven isolates representing two previously undescribed species, along with 93 high-quality metagenome-assembled genomes (MAGs) derived from a global survey across five continents. Phylogenomic analysis revealed 16 species forming nine distinct biogeographic clusters, indicating speciation patterns linked to water temperature and latitude. We observed endemic species restricted to African lakes, and quasi-endemic species confined to the Northern or Southern Hemisphere, which co-exist alongside cosmopolitan species. Metabolic profiling and growth experiments uncovered species- and strain-specific adaptations for nutrient uptake, along with unique pathways for sulfur metabolism. These findings provide a global-scale genomic and ecological overview for this underexplored lineage of freshwater SAR11.

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Fig. 1: Phylogeny of the SAR11 order.
Fig. 2: Global occurrence of different Fontibacterium species.
Fig. 3: Seasonal distribution of different Fontibacterium species.
Fig. 4: Growth of two Fontibacterium species under different experimental conditions.
Fig. 5: Metabolic pathways of seven Fontibacterium strains.

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Data availability

Genomes from cultures have been submitted to ENA under project accession number PRJEB77526, Illumina and Oxford Nanopore reads, and MAGs under ENA project accession numbers PRJEB35770 and PRJEB86000–PRJEB86004. Novel species were registered at SeqCode29 in register lists seqco.de/r:gnukuc44 and seqco.de/r:opjv7zsc. Phylogenomic and phylogenetic trees are available in iTOL (https://itol.embl.de/shared/2Kl1yRwH6Azmk). Strains can be requested by email to M.M.S. (michaelasalcher@gmail.com). All commercial interests in the data from Lake Malawi are reserved by the Government of Malawi; any proposed commercial use requires negotiation of a separate agreement by the intended user with the Government of Malawi, according to an ABS contract between the Government of the Republic of Malawi and the Biology Centre of the Czech Academy of Sciences.

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Acknowledgements

We thank local fisherman, captains and technicians, and S. Sho, M. Zalewski, A. Woźniczka, P. Znachor, P. Rychtecký, P. Pejsar, V. Lanta, C. Callieri, F. Lepori, S. Mayer, A. Kust, B. Sonntag, E. Loher, J. Pernthaler and T. Posch for help during sampling. The Government of Malawi and the Department of Fisheries (Ministry of Natural Resources and Climate Change, Lilongwe, Malawi) are acknowledged for issuing sampling and export permits to take samples from Lake Malawi; the Department of Environment and Science, Queensland Government, Australia for issuing a permit to sample lakes on K’gari (Fraser Island, Great Sandy National Park), and the Butchulla Aboriginal Corporation for allowing us to take samples from lakes on K’gari. Sample collection in Lake Biwa was supported by the Center for Ecological Research, Kyoto University, a Joint Usage/Research Center and the research vessel ‘Hasu’. Sampling in Lake Toya was supported by a joint usage with Toya Lake Station of the Field Science Center for Northern Biosphere, Hokkaido University. F. Kostanjšek, M. Okrouhliková, A. Férová and I. Lebeda are acknowledged for excellent laboratory support. We thank the Biology Centre CAS core facility LEM supported by MEYS CR (LM2023050 Czech-BioImaging and OP VVV CZ.02.1.01/0.0/0.0/18_046/0016045). This study was mainly supported by Czech Science Foundation (GAČR) grants. Grants 22-03662S and 25-15813S were awarded to M.M.S. and supported C.F, M.H., P.L., M.-C.C. and M.M.S. Grant 21-21990S was awarded to M.H. and supported M.-C.C. and M.H. Grant 20-12496X was awarded to R.G. and supported R.G., P.-A.B. and V.K. C.F. and P.L. also received support from the Grant Agency of the University of South Bohemia in České Budějovice (grants 017/2022/P to C.F. and 022/2019/P to P.L.). J.W. and H.-P.G. were funded by the Leibniz foundation, a German Science Foundation grant (GR1540/37-1 to H.-P.G.), and thank the entire LIMNOS team. Y.O. was funded by JST FOREST programme (JPMJFR2273) and JSPS KAKENHI grants (16H06279, 18J00300, 22K15182).

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Authors and Affiliations

  1. Institute of Hydrobiology, Biology Centre CAS, Ceske Budejovice, Czech Republic

    Clafy Fernandes, Markus Haber, Paul Layoun, Maria-Cecilia Chiriac, Paul-Adrian Bulzu, Rohit Ghai, Vojtech Kasalicky, Tanja Shabarova & Michaela M. Salcher

  2. Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic

    Clafy Fernandes & Paul Layoun

  3. Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Stechlin, Germany

    Hans-Peter Grossart & Jason Woodhouse

  4. Institute of Biochemistry and Biology, Potsdam University, Potsdam, Germany

    Hans-Peter Grossart

  5. Department of Fisheries Oceanography and Marine Ecology, National Marine Fisheries Research Institute, Gdynia, Poland

    Kasia Piwosz

  6. Centro Universitario de la Región Este, Universidad de la República, Rocha, Uruguay

    Cecilia Alonso & Juan Zanetti

  7. Australian Rivers Institute, Griffith University, Queensland, Australia

    David P. Hamilton

  8. Department of Fisheries, Lilongwe, Malawi

    Maxon Ngochera

  9. Center for Ecological Research, Kyoto University, Kyoto, Japan

    Shin-ichi Nakano

  10. Institute for Chemical Research, Kyoto University, Kyoto, Japan

    Yusuke Okazaki

Authors
  1. Clafy Fernandes
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  2. Markus Haber
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  3. Paul Layoun
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  4. Maria-Cecilia Chiriac
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  5. Paul-Adrian Bulzu
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  6. Rohit Ghai
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  7. Vojtech Kasalicky
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  8. Tanja Shabarova
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  9. Hans-Peter Grossart
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  10. Jason Woodhouse
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  11. Kasia Piwosz
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  12. Cecilia Alonso
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  13. Juan Zanetti
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  14. David P. Hamilton
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  15. Maxon Ngochera
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  16. Shin-ichi Nakano
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  17. Yusuke Okazaki
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  18. Michaela M. Salcher
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Contributions

M.M.S. conceived the study. Sampling was performed by C.F., M.H., P.L., M.-C.C., R.G., V.K., T.S., H.-P.G., J.W., K.P., C.A., J.Z., D.P.H., M.N. S.N., Y.O. and M.M.S. C.F., M.H., P.L. and M.M.S. isolated and maintained the strains, and C.F. conducted growth assays. C.F., M.-C.C., P.-A.B. and M.M.S. assembled, binned and annotated the metagenomes with pipelines designed by P.-A.B. and R.G. C.F. analysed the data and prepared the figures, supervised by M.M.S. C.F. and M.M.S. wrote the manuscript with input from all authors.

Corresponding author

Correspondence to Michaela M. Salcher.

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Competing interests

The authors declare no competing interests.

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Nature Microbiology thanks Luis Rodriguez-R and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Map displaying the origin of Fontibacterium genomes.

Global distribution of sampling locations for Fontibacterium genomes. Yellow stars and green circles indicate new culture genomes and high-quality MAGs, respectively, retrieved in this study from a. Europe, b. Japan, c. Uruguay, d. Malawi and e. Australia. Red circles indicate genomes from public databases and a red star indicates the culture F. commune LSUCC0530.

Extended Data Fig. 2 Genome synteny and genomic islands in complete genomes of Fontibacterium spp.

a. Whole-genome alignments and BLASTp comparisons of all complete Fontibacterium genomes analyzed in this study. The hypervariable region 2 (HVR2) in between 16S-23S rRNA and 5S rRNA appears conserved in the genus. Genomes are sorted according to taxonomy as follows: F. medardense (ME-31, ME-33, ME-17, ME-20, ME-18), F. abundans (30–26, MiE-29, MKE-138), F. lacus (N-BarE-26apr23-C31), F. commune (LSUCC0530), tRNA and rRNA genes are indicated by short lines. b. Zoom-in of the first few genes in HVR2 of strain ME-20. Genes involved in sulfate reduction (cysD, cysNC) and cysteine biosynthesis (cysE) are highlighted in yellow.

Extended Data Fig. 3 Average nucleotide identities (ANI, %) within each species of Fontibacterium and ANI to the closest relative.

Boxplots showing average nucleotide identities (ANI, %) within each species of Fontibacterium and max. ANI to the closest relative. Boxes indicate the 25th and 75th quantiles, medians are displayed by central lines, whiskers indicate the 5th and 95th quantiles. ANI values to the closest relative from another species group are displayed as red dots and lines. The number of genomes used for ANI comparisons (n) is indicated above the plot.

Extended Data Fig. 4 Genome synteny plot of Fontibacterium species.

Whole-genome alignments and BLASTn comparisons of one to two representatives per Fontibacterium species and all complete genomes analyzed in this study. Genomes are sorted according to taxonomy and colour-coded as in Fig. 1. Asterisks indicate complete genomes; all others were concatenated in order based on the closest complete relative and turned to start with DnaA for an easier display of synteny and nucleotide identity. Note that nucleotide identities >95% were rarely detected between different species and that HVR2 (located at approx. 0.1-0.2 Mb) was not assembled in multiple MAGs.

Extended Data Fig. 5 Clustering of SAR11-IIIb.1-16 species based on coverage per Gb values in metagenomes.

a. Non-metric multidimensional scaling (NMDS) plot showing distinct clusters based on metagenomic fragment recruitment values (n = 307). Points in the NMDS plot represent species that are coloured and shaped according to their assigned cluster (stress value: 0.071). b. The corresponding dendrogram from hierarchical clustering (Ward’s linkage method); with observed clusters highlighted by black rectangles. Nine optimal clusters were identified, with the number of clusters determined by average silhouette width (Supplementary Fig. 2) and dendrogram evaluation. Raw data can be found in Supplementary Table 6.

Extended Data Fig. 6 Latitudinal variation across the SAR11-IIIb clusters.

Box plots show the latitudinal distribution for each of the nine distinct clusters identified from n = 307 metagenomes (see Extended Data Fig. 5). The number of individual metagenomes assigned to each cluster (n) is indicated below the x-axis label. Box plots display the median (center line) and interquartile range (IQR; box), and whiskers extend to the furthest data point within 1.5 × IQR of the hinge, with outliers plotted individually. An overall difference in latitude among the nine clusters was tested using a Kruskal-Wallis test (P = 2.2e-16).

Extended Data Fig. 7 Redundancy analysis (RDA) ordination plots of the seasonal distribution of SAR11-IIIb species in six lakes in relation to environmental variables.

Redundancy analysis (RDA) biplots showing the relationship between the dominant SAR11-IIIb species (red circles), seasonal sampling points (yellow circles), and significant environmental variables (arrows). Key environmental factors were identified through forward selection (P < 0.05). The model was statistically significant (ANOVA, P < 0.001, 999 permutations). Abbreviations: Temp, water temperature (°C); Chla, chlorophyll a (µg l−1); Total.Chl, Total chlorophyll (µg l−1); SRP, soluble reactive phosphorus (µg l⁻¹); NO₃, nitrate (mg l−1); NO₂, nitrite (mg l−1); npoc, non-purgeable particulate organic carbon; TP, total phosphorus (µg l−1); TN, total nitrogen (mg l−1); DOC, dissolved organic carbon (mg l−1); R-Si, dissolved reactive silica (mg l−1); DO, dissolved oxygen (mg l−1). Raw data can be found in Supplementary Tables 7 and 9, results of statistical tests in Supplementary Table 9.

Extended Data Fig. 8 Growth of two Fontibacterium species under different experimental conditions.

Maximum abundances (a-d) and growth rates (e-h) of F. medardense ME-17 and F. abundans MiE-29. a,e: Different media (med2, 3 and 5); b,f: Sulfur-amino acids (cysteine and methionine) concentrations (0.1, 0.5, 1 and 5 µM); c,g: Oxaloacetate concentrations (0.1, 0.5, 1 and 5 µM) d,h: Pyruvate concentrations (0.1, 0.5, 1 and 5 µM). Shown are means of triplicates, error bars represent standard errors, individual samples are displayed as red dots. Letters indicate significant differences between treatments; blue asterisks indicate significant differences between strains based on ANOVA and post-hoc tests (Turkey-HSD). Raw data can be found in Supplementary Table 11, results of statistical tests in Supplementary Tables 12 and 13.

Extended Data Fig. 9 Phylogenetic tree of isocitrate lyase (AceA).

a. Full tree of 1367 AceA protein sequences from all bacterial phyla, the SAR11 clade is highlighted in red. b. Subtree of SAR11 AceA protein sequences and closely related taxa.

Extended Data Fig. 10 Phylogenetic trees of proteins involved in sulfate reduction (CysD, CysNC) and cysteine biosynthesis (CysE) present in HVR2 of F. medardense ME-20.

a. Phylogenetic tree of O-acetylhomoserine (thiol)-lyase CysD including 100 closely related protein sequences. b. Phylogenetic tree of sulfate adenylyltransferase CysNC including 100 closely related protein sequences. c. Phylogenetic tree of serine O-acetyltransferase CysE including 100 closely related protein sequences. Accession numbers are colour-coded by taxonomy and collapsed at order level. The habitat of origin of ‘Ca. Pelagibacterales’ is indicated by different colours.

Supplementary information

Supplementary Information

Supplementary Text (additional findings and discussion, SeqCode descriptions of new species, supplementary references) and Figs. 1–4.

Reporting Summary

Peer Review File

Supplementary Tables

Supplementary Table 1. Sampling details for newly sequenced metagenomes. Table 2. Details on genomes used in this study. Table 3. List of TIGRFAMs used for phylogenomic tree reconstruction. Table 4. Average nucleotide identity (ANI) matrix of all genomes used in this study. Table 5. Average amino acid identity (AAI) matrix of all genomes used in this study. Table 6. Metagenomic fragment recruitment results for 16 Fontibacterium species. Table 7. Metagenomic fragment recruitment results for 16 Fontibacterium species in time-series metagenomes. Table 8. Physico-chemical data for time-series metagenomes. Table 9. Statistical tests for seasonal distribution of Fontibacterium species. Table 10. Media components. Table 11. Raw data of growth assays conducted in this study. Table 12. ANOVA and post hoc tests (Turkey-HSD) for growth assays based on maximum abundances. Table 13. ANOVA and post hoc tests (Turkey-HSD) for growth assays based on maximum growth rates. Table 14. Overview of metabolic pathways present in the culture genomes. Table 15. Presence/absence of individual KEGG IDs (metabolic pathways) detected in different Fontibacterium species.

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Fernandes, C., Haber, M., Layoun, P. et al. Ecophysiology and global dispersal of the freshwater SAR11-IIIb genus Fontibacterium. Nat Microbiol 10, 2194–2206 (2025). https://doi.org/10.1038/s41564-025-02091-8

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