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Background <p>The order&#xa0;<i>Nanopelagicales</i> is the most abundant bacterioplankton lineage in freshwater lakes and exhibits typical streamlined genomic characteristics such as small cell volumes (&lt;0.1 μm<sup>3</sup>), reduced genome sizes (&lt;1.5 Mbp), and low GC content. These characteristics reflect adaptations to a free-living life strategy in oligotrophic environments. While many <i>Nanopelagicales</i> metagenome-assembled genomes and single-amplified genomes are available in public databases, strain-level microdiversity within this lineage remains poorly understood. This is mainly attributed to the incomplete nature of these genomes and the difficulty in isolating and maintaining pure cultures, with only 20 genome-sequenced cultures available to date.</p> Results <p>Here, we report the isolation and genome analysis of 72 new <i>Nanopelagicales</i> strains, including members of <i>Planktophila</i> and a novel, previously uncultured genus, <i>Aquilimus.</i> High interspecific diversity and microdiversity were observed in the&#xa0;genus <i>Planktophila</i>, which likely facilitates the coexistence of closely related species within the same habitats by allowing fine-scale niche partitioning. The unusually high diversity of transporters for small organic compounds, along with carbohydrate-active enzymes, suggests that <i>Planktophila</i> members can degrade plant and algal polymers and import the resulting products to support growth. A notable finding is the repeated, independent loss of the oxidative phase of the pentose phosphate pathway in abundant <i>Nanopelagicales</i> species, which may represent an energy-saving adaptation in oligotrophic waters. Two species (<i>Planktophila vernalis</i> and <i>Nanopelagicus abundans</i>) seem to be equally abundant on a global scale, with water pH likely being the most significant factor influencing the predominance of one group over the other in different water bodies. Additionally, <i>P. vernalis</i> may tolerate periods of anoxia due to genomic encoding of respiratory nitrate reductase and nitrate/nitrite antiporters.</p> Conclusions <p>In conclusion, this work increased to a great degree the cultivated diversity of the abundant <i>Nanopelagicales</i> order. Analysis of over 1700 metagenomes showed that only a few cultivated species are globally dominant, and time-series analyses revealed consistent spring and autumn peaks. Key metabolic adaptations, such as loss of the oxidative phase of the pentose phosphate pathway and a high microdiversity of genes involved in cell surface biosynthesis and modifications, are likely to help these species survive periods of starvation and avoid predation. These findings highlight the ecological importance of <i>Nanopelagicales</i> and suggest that microdiversity underpins their adaptability. This work lays a foundation for studying their physiology, ecology, and strain-specific functional variation.</p> <p><MediaObject ID="MOESM4"> <VideoObject FileRef="MediaObjects/40168_2025_2272_MOESM4_ESM.mp4" VideoID="Bt8hQzKWva2FEq-Hh1AjGA"> <Caption Language="En" xml:lang="en"> <CaptionContent> <p>Video Abstract</p> </CaptionContent> </Caption> </VideoObject> </MediaObject></p>

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Ecological success in freshwater lakes: insights from novel cultivated lineages of the abundant Nanopelagicales order

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年12月12日

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  • Maria-Cecilia Chiriac,
  • Paul Layoun,
  • Clafy Fernandes,
  • Tiberiu Szőke-Nagy,
  • Vojtech Kasalicky,
  • Yusuke Okazaki,
  • Jason N. Woodhouse,
  • Hans-Peter Grossart,
  • Kasia Piwosz,
  • Petr Znachor,
  • Bettina Sonntag,
  • Cristiana Callieri,
  • Sandi Orlić,
  • Ruben Sommaruga,
  • Cécile Lepère,
  • Corinne Biderre-Petit,
  • Helen Tammert,
  • Daniel P. R. Herlemann,
  • Mirosław Ślusarczyk,
  • Anna Bednarska,
  • Horia L. Banciu,
  • Mariusz Zalewski,
  • Adam Woźniczka,
  • Rohit Ghai,
  • Michaela M. Salcher,
  • Markus Haber

摘要

Background

The order Nanopelagicales is the most abundant bacterioplankton lineage in freshwater lakes and exhibits typical streamlined genomic characteristics such as small cell volumes (<0.1 μm3), reduced genome sizes (<1.5 Mbp), and low GC content. These characteristics reflect adaptations to a free-living life strategy in oligotrophic environments. While many Nanopelagicales metagenome-assembled genomes and single-amplified genomes are available in public databases, strain-level microdiversity within this lineage remains poorly understood. This is mainly attributed to the incomplete nature of these genomes and the difficulty in isolating and maintaining pure cultures, with only 20 genome-sequenced cultures available to date.

Results

Here, we report the isolation and genome analysis of 72 new Nanopelagicales strains, including members of Planktophila and a novel, previously uncultured genus, Aquilimus. High interspecific diversity and microdiversity were observed in the genus Planktophila, which likely facilitates the coexistence of closely related species within the same habitats by allowing fine-scale niche partitioning. The unusually high diversity of transporters for small organic compounds, along with carbohydrate-active enzymes, suggests that Planktophila members can degrade plant and algal polymers and import the resulting products to support growth. A notable finding is the repeated, independent loss of the oxidative phase of the pentose phosphate pathway in abundant Nanopelagicales species, which may represent an energy-saving adaptation in oligotrophic waters. Two species (Planktophila vernalis and Nanopelagicus abundans) seem to be equally abundant on a global scale, with water pH likely being the most significant factor influencing the predominance of one group over the other in different water bodies. Additionally, P. vernalis may tolerate periods of anoxia due to genomic encoding of respiratory nitrate reductase and nitrate/nitrite antiporters.

Conclusions

In conclusion, this work increased to a great degree the cultivated diversity of the abundant Nanopelagicales order. Analysis of over 1700 metagenomes showed that only a few cultivated species are globally dominant, and time-series analyses revealed consistent spring and autumn peaks. Key metabolic adaptations, such as loss of the oxidative phase of the pentose phosphate pathway and a high microdiversity of genes involved in cell surface biosynthesis and modifications, are likely to help these species survive periods of starvation and avoid predation. These findings highlight the ecological importance of Nanopelagicales and suggest that microdiversity underpins their adaptability. This work lays a foundation for studying their physiology, ecology, and strain-specific functional variation.

Video Abstract