Femtoplankton: What's New?

Abstract

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.

Keywords: aster-like nanoparticles; biomimetic mineral–organic particles; extracellular vesicles; femtoplankton; gene transfer agents; ultra-small prokaryotes; viruses.

Figure 1

Schematic representation of plankton size classes (adapted from [2]).

Figure 2

Transmission electron micrographs of biomimetic mineral–organic- (BMOPs) and/or nanobe-like particles (A–H) and vesicle-like particles (I–S). Arrows indicate the target particles when the samples are heterogeneous. (A,B,N–S) scale bar: 100 nm, (C–H,I–M) scale bar: 500 nm.

Figure 3

Transmission electron micrographs of different morphotypes of virus-like particles (VLPs). (A) VLP embedded in a vesicle-like structure. (B) Tailless VLP. (C–N) Tailed VLPs representing phages like morphotypes. (O–U) Giant tailed VLPs. (V–Y) Archaea-like viruses. Scale bars = 100 nm, excepted notifications (O,S,R).

Figure 4

Transmission electron micrographs of attached (A–Q) or free (R–T) femtoplankton-like prokaryotes. Arrows indicate the target particles when the samples are heterogeneous. Scale bar: 500 nm.

Figure 5

Transmission electron micrographs of different morphotypes of aster-like nanoparticles (ALNs). (A–H) 4–10-armed forms. (I–M) 11-armed forms and their budding 11-armed variants (N–R) with elongated and swollen bud-like excrescences. (S–X) 20-armed forms. Scale bars = 100 nm.

Figure 6

Schematic overview of the main components and of organizational complexity (increase in complexity from left to right) of the femtoplankton entities mentioned in this review. The question mark (?) represent uncertainty about the presence/absence of this compound in the target entity. The dotted line (--) means “Optional”. GTAs = gene transfer agents, BMOPs = Biomimetic mineral–organic particles, ALNs = aster-like nanoparticles. Note that the tail (mainly an attribute of bacteriophages) is not present in all naked viruses.

Figure 7

Significance of femtoplankton entities in prebiotic evolution: a potential pathway to the cellular and viral world. Early stages of evolution leading to a procell are based on the hypothesis of a prebiotic peptide/RNA world developed in [181]. In these early stages biomimetic mineral–organic particles (BMOPs)/nanobes, as a potential support (inside or fixed outside) of prebiotic organic chemistry, could have paved the way for the formation of organic molecules. The evolution of a procell toward the first protocell can be achieved after encapsulation and compartmentalization of the primitive elements into fatty acid vesicles prior to evolution by unregulated and error-prone way division, depending on environmental conditions [47,182]. Complexification of biochemical (metabolic) and replicative systems, as well as membrane/cell walls, during the protocell stages has led to divisions that are more independent of environmental conditions [182] and to the initiation of the cellular and viral world [94]. The emergence of Candidate Phyla Radiation/Diapherotrites Parvarchaeota Aenigmarchaeota Nanoarchaeota Nanohaloarchaeota (CPR/DPANN) from protocell or prokaryotic communities is adapted from [165].

Figure 8

Schematic overview of the specific and major ecological roles of femtoplankton entities mentioned in this review. BMOPs = Biomimetic mineral–organic particles, ALNs = aster-like nanoparticles, CPR/DPANN = Candidate Phyla Radiation/Diapherotrites Parvarchaeota Aenigmarchaeota Nanoarchaeota Nanohaloarchaeota, GTAs = gene transfer agents, HGT = horizontal gene transfers.