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

Chiriac, Maria-Cecilia; Layoun, Paul; Fernandes, Clafy; Szőke-Nagy, Tiberiu; Kasalicky, Vojtech; Okazaki, Yusuke; Woodhouse, Jason N.; Grossart, Hans-Peter; Piwosz, Kasia; Znachor, Petr; Sonntag, Bettina; Callieri, Cristiana; Orlić, Sandi; Sommaruga, Ruben; Lepère, Cécile; Biderre-Petit, Corinne; Tammert, Helen; Herlemann, Daniel P. R.; Ślusarczyk, Mirosław; Bednarska, Anna; Banciu, Horia L.; Zalewski, Mariusz; Woźniczka, Adam; Ghai, Rohit; Salcher, Michaela M.; Haber, Markus (2025) Ecological success in freshwater lakes: insights from novel cultivated lineages of the abundant Nanopelagicales order. Microbiome, 14 (1). ISSN 2049-2618

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Abstract

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.

Item Type:	Article
Uncontrolled Keywords:	Aquilimus; Bacterial cultivation; Genomics; Microdiversity; Nanopelagicales; Nanopelagicus; Planktophila; Seasonal variation
Subjects:	NATURAL SCIENCES
Divisions:	Division of Materials Chemistry
Projects:	Project title Project leader Project code Project type STIM-REI (hrv. istraživanje, inovacija, edukacija)-STIM-REI Vlasta Bonačić-Koutecky KK.01.1.1.01.0003 EK Mikrobna ekologija jezerskih ekosutava - novi pristup-MALENA Sandi Orlić IP-2020-02-9021 HRZZ
Depositing User:	Ana Zečević
Date Deposited:	20 May 2026 08:21
URI:	https://fulir.irb.hr:/id/eprint/11975
DOI:	10.1186/s40168-025-02272-x

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