Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function

Abstract

Nano-sized and filterable microorganisms are thought to represent the smallest living organisms on earth and are characterized by their small size (50-400 nm) and their ability to physically pass through <0.45 μm pore size filters. They appear to be ubiquitous in the biosphere and are present at high abundance across a diverse range of habitats including oceans, rivers, soils, and subterranean bedrock. Small-sized organisms are detected by culture-independent and culture-dependent approaches, with most remaining uncultured and uncharacterized at both metabolic and taxonomic levels. Consequently, their significance in ecological roles remain largely unknown. Successful isolation, however, has been achieved for some species (e.g., Nanoarchaeum equitans and "Candidatus Pelagibacter ubique"). In many instances, small-sized organisms exhibit a significant genome reduction and loss of essential metabolic pathways required for a free-living lifestyle, making their survival reliant on other microbial community members. In these cases, the nano-sized prokaryotes can only be co-cultured with their 'hosts.' This paper analyses the recent data on small-sized microorganisms in the context of their taxonomic diversity and potential functions in the environment.

Keywords: copiotrophy; filterable microorganisms; nano-sized microorganisms; oligotrophy; ultramicrocells; unculturable.

FIGURE 1

Summary of definitions used to describe nano-sized organisms: (A) microorganisms shrinking in body size, (B) consistently small-bodied microorganisms and (C) large microorganisms that pass through filters. References are the following: [1] Duda et al., 2012; [2] Velimirov, 2001; [3] Panikov, 2005; [4] Schut et al., 1995; [5] Miteva and Brenchley, 2005; [6] Luef et al., 2015; [7] Huber et al., 2002; [8] Rogge et al., 2017; [9] Giovannoni, 2017; [10] Kajander and Ciftcioglu, 1998; [11] Fedotova et al., 2012.

FIGURE 2

Surface area (SA) and volume (V) ratios in three selected species of different sizes: Escherichia coli, “Candidatus Pelagibacter ubique,” and Nanoarchaeum equitans. The microorganism with the smallest dimensions (“Ca. P. ubique”) had the largest ratio at 22. The habitat of “Ca. P. ubique” is the open ocean (oligotrophic environment) and hence its high SA/V ratio is advantageous to living in low nutrient conditions. The total protein numbers in encoded by genomes of E. coli (NCBI Reference Sequence: NC_000913.3), “Ca. P. ubique” (GenBank: CP000084.1), and N. equitans (GenBank: AE017199.1) are given and related with the proteins with membrane-spanning domains. For prediction of transmembrane helices in proteins, above genomes were analyzed using TMMHMM 2.0 Server at http://www.cbs.dtu.dk/services/TMHMM/ (Krogh et al., 2001; Möller et al., 2001). ^∗Dimensions and calculations of surface area and volume were obtained from Young (2006). ^∗∗The diameter was obtained from Huber et al. (2002), the equations for the surface area (SA = 4πr², where r is the radius) and volume $\mathrm{V}\mathrm{=}\frac{\mathrm{4}}{\mathrm{3}}\mathrm{\pi }{\mathrm{r}}^{\mathrm{3}}$, where r is the radius) of a sphere.

FIGURE 3

Size comparison of nano-sized organisms. Each of the colored lines represents relative range of sizes (in one dimension) of each individual. References and numerical ranges for individuals can be found in Table 1. If size was reported with volume, the organism was assumed to be spherical and then obtained the radius with the equation, $\mathrm{V}\mathrm{=}\frac{\mathrm{4}}{\mathrm{3}}\mathrm{\pi }{\mathrm{r}}^{\mathrm{3}}$, where r is the radius. ^∗References for size guides: Escherichia coli (approximately 1 μm × 2 μm) and phage T4 (approximately 90 nm × 200 nm) (Leiman et al., 2003). ‘Ca. Nanobsidianus stetteri’ has no available information concerning cellular dimensions.