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The smallest entities in aquatic ecosystems, i.e., femtoplankton, are certainly the largest reservoir of uncharacterized biodiversity. Among them, the discovery of mysterious Aster like nanoparticles has raised many questions about their nature, origin and ecology. Here, we highlight the original nature of this new model, organic and composed of enriched-calcium carbohydrates, with no detection of nucleic acids or proteins. The biosynthesis of these entities seems to be associated with a host in their 11 arms’ form prior to their release into the environment. An intriguing aspect of their mode of development is their ability, once free, to change form and maintain their abundance autonomously without metabolism being detected, resulting in an unexpected polymorphism. Their remarkable capacity for massive in situ development and their links with prokaryotes and other microbes suggest a major role in the functioning of aquatic ecosystems. There’s no doubt that these new entities are a source of new knowledge not only in the sciences of organic nanoparticles, but also in their ecological importance for aquatic ecosystems.

Since the discovery of high abundances of virus-like particles in aquatic environment, emergence of new analytical methods in microscopy and molecular biology has allowed significant advances in the characterization of the femtoplankton, i.e., floating entities filterable on a 0.2 µm pore size filter. The successive evidences in the last decade (2010–2020) of high abundances of biomimetic mineral–organic particles, extracellular vesicles, CPR/DPANN (Candidate phyla radiation/Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota), and very recently of aster-like nanoparticles (ALNs), show that aquatic ecosystems form a huge reservoir of unidentified and overlooked femtoplankton entities. The purpose of this review is to highlight this unsuspected diversity. Herein, we focus on the origin, composition and the ecological potentials of organic femtoplankton entities. Particular emphasis is given to the most recently discovered ALNs. All the entities described are displayed in an evolutionary context along a continuum of complexity, from minerals to cell-like living entities.

Laboratory incubations of natural microbial communities can aid in the study of member organisms and their networks of interaction. This is particularly important for understudied lineages for which key elements of basic biology are still emerging. Microbial communities in lakes can profoundly impact biogeochemical processes through their individual activities and collective interactions. However, the complexity of these communities poses challenges, particularly for studying rare organisms such as Candidate Phyla Radiation bacteria (CPR) and enigmatic entities such as aster-like nanoparticles (ALNs). Here, a reactor was inoculated with water from Lake Fargette, France, and maintained under dark conditions at 4°C for 31 months and enriched for ALNs, diverse Planctomycetes , and CPR bacteria. We reconstructed draft genomes and predicted metabolic traits for 12 diverse Planctomycetes and 9 CPR bacteria, some of which are likely representatives of undescribed families or genera. One CPR genome representing the little-studied lineage “ Candidatus Peribacter” was curated to completion (1.239 Mbp) and unexpectedly encodes the full gluconeogenesis pathway. Metatranscriptomic data indicate that some planctomycetes and CPR bacteria were active under the culture conditions, accounting for ∼30% and ∼1% of RNA reads mapping to the genome set, respectively. We also reconstructed genomes and obtained transmission electron microscope images for numerous viruses, including one with a >300-kbp genome and several predicted to infect Planctomycetes . Together, our analyses suggest that freshwater Planctomycetes are central players in a subsystem that includes ALNs, symbiotic CPR bacteria, and viruses. IMPORTANCE Laboratory incubations of natural microbial communities can aid in the study of member organisms and their networks of interaction. This is particularly important for understudied lineages for which key elements of basic biology are still emerging. Using genomics and microscopy, we found that members of the bacterial lineage Planctomycetes may be central players in a subset of a freshwater lake microbiome that includes other bacteria, archaea, viruses, and mysterious entities, called aster-like nanoparticles (ALNs), whose origin is unknown. Our results help constrain the possible origins of ALNs and provide insight into possible interactions within a complex lake ecosystem.

Under the effect of global change, management of cyanobacterial proliferation becomes increasingly pressing. Given the importance of interactions within microbial communities in aquatic ecosystems, a handful of studies explored the potential relations between cyanobacteria and their associated bacterial community (i.e., cyanosphere). Yet, most of them specifically focused on the ubiquitous cyanobacteria Microcystis , overlooking other genera. Here, based on 16s rDNA metabarcoding analysis, we confirmed the presence of cyanosphere representing up to 30% of the total bacterial community diversity, during bloom episode of another preponderant cyanobacterial genus, Dolichospermum . Moreover, we highlighted a temporal dynamic of this cyanosphere. A sPLS-DA model permits to discriminate three important dates and 220 OTUs. With their affiliations, we were able to show how these variations potentially imply a turnover in ecological functions depending on bloom phases. Although more studies are necessary to quantify the impacts of these variations, we argue that cyanosphere can have an important, yet underestimated, role in the modulation of cyanobacterial blooms.

Aster-like nanoparticles (ALNs) are femtoentities, recently discovered in different aquatic environments, whose intrinsic nature and ecological features remain to be determined. In this study, we investigate the in situ temporal dynamics of ALNs during 1 year in 3 different lakes, in relation to the physico-chemical and biological environment. ALN abundances in investigated lakes showed a marked seasonal dynamic (from no detectable to 4.28 ± 0.75 × 10 6 ALNs mL −1 ), with characteristic peaks in spring. We recorded a correlation between ALNs and some prokaryotic phyla suggesting a broad and non-specific relationship. From their seasonal dynamics and potential link with prokaryotes, we conclude that ALNs represent an important ecological actor in the functioning of aquatic ecosystems.

The discovery of jumbo phages and giant viruses of microeukaryotes has transformed our perception of the virosphere. Metagenomic and metatranscriptomic data further highlight their diversity and ecological impact. Nevertheless, sequence-based approaches fail to take into account the morphological diversity of non-cultivated viruses, resulting in our fragmented understanding of their nature and role in the environment. Here, we combined flow cytometry and electron microscopy to uncover both previously unsuspected morphological diversity and significant abundances of large virus-like particles in aquatic environments. We discovered new viral morphotypes, all likely to be associated with microeukaryotes. We also obtained insights into the multi-year dynamics of the abundances of both giant microeukaryotic virus-like particles and jumbo phage-like particles. This work deepens our understanding of large virus and reveals their key role as regulators of microbial communities.

Aster-like nanoparticles (ALNs) are newly described femto-entities. Their ecology (e.g., geographic distribution, spatial dynamic, preferences, forcing factors) is still unknown. Here, we report that these entities, which have largely been ignored until now, can develop or maintain themselves in most aquatic environments in the Loire River catchment, France. We observed a significant influence of the trophic state on ALN ecological distributions. A positive relationship between prokaryotic abundance and ALN (r(2) = 0.72,p < 0.01) has been identified, but its exact nature remains to be clarified. Combined with their ubiquitous distribution and high abundances (up to 7.9 x 10(6) ALNs mL(-1)) recorded in our samples, this probably makes ALNs an overlooked functional component in aquatic ecosystems.

Aster-like nanoparticles (ALNs) are newly described femto-entities. Their ecology (e.g., geographic distribution, spatial dynamic, preferences, forcing factors) is still unknown. Here, we report that these entities, which have largely been ignored until now, can develop or maintain themselves in most aquatic environments in the Loire River catchment, France. We observed a significant influence of the trophic state on ALN ecological distributions. A positive relationship between prokaryotic abundance and ALN (r(2) = 0.72,p < 0.01) has been identified, but its exact nature remains to be clarified. Combined with their ubiquitous distribution and high abundances (up to 7.9 x 10(6) ALNs mL(-1)) recorded in our samples, this probably makes ALNs an overlooked functional component in aquatic ecosystems.

Global change severely increases the recurrence of freshwater cyanobacterial proliferations, with known deleterious consequences for ecosystem structure and functioning. A few studies highlighted the existence of bacterial communities associated to cyanobacteria (i.e., Cyanosphere), comparable to the well-known phycosphere. While phycosphere in general is expected to exchange nutrients with their associated phytoplankton communities, specific functions and dynamic of the cyanosphere remain unknown. Here, based on metabarcoding approaches, we showed that during bloom episodes, cyanosphere accounts for up to 30% of total bacterial abundance. More importantly, we demonstrated for the first-time the dynamics aspect of cyanosphere community composition at crucial bloom phases. In our study, these community changes imply variations in cyanosphere ecological functions over time. Our results highlight the ability of cyanosphere to regulate nutrient and energy exchange with cyanobacteria during the entire bloom period, modulating bloom intensity and dynamics. In the latter bloom phases, cyanosphere additionally tends to create microhabitats favoring cyanobacterial persistence in deleterious environmental conditions. At wider scale, as blooms constitute major turnovers of matter and energy in aquatic ecosystems, we argue that cyanosphere can have an important, yet underestimated, role in mediating C and nutrient cycles in environments.

The discovery of Jumbo phages and giant viruses of microeukaryotes has transformed our perception of the virosphere. Metagenomic and metatranscriptomic data further highlight their diversity and ecological impact. Nevertheless, sequence-based approaches fail to take into account the morphological diversity of non-cultivated viruses, resulting in our fragmented understanding of their nature and role in the environment. Here, we combined flow cytometry and electron microscopy to uncover both previously unsuspected morphological diversity as well as significant abundances of large viruses in aquatic environments. We discovered four new viral morphotypes, all of which were associated with microeukaryotes. We also obtained insights into the multi-year dynamics of the abundances of both giant microeukaryotic viruses and Jumbo phages. This work deepens our understanding of large viruses and reveals their key role as regulators of microbial communities.