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Nano-Sized and Filterable Bacteria and Archaea Nano-Sized and Filterable Bacteria and Archaea ANGOR UNIVERSITY Ghuneim, Lydia-Ann; Jones, Davey L.; Golyshin, Peter; Golyshina, Olga Frontiers in Microbiology DOI: 10.3389/fmicb.2018.01971 PRIFYSGOL BANGOR / B Published: 21/08/2018 Publisher's PDF, also known as Version of record Cyswllt i'r cyhoeddiad / Link to publication Dyfyniad o'r fersiwn a gyhoeddwyd / Citation for published version (APA): Ghuneim, L-A., Jones, D. L., Golyshin, P., & Golyshina, O. (2018). Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function. Frontiers in Microbiology, 9, [1971]. https://doi.org/10.3389/fmicb.2018.01971 Hawliau Cyffredinol / General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. 29. Sep. 2021 fmicb-09-01971 August 18, 2018 Time: 18:55 # 1 REVIEW published: 21 August 2018 doi: 10.3389/fmicb.2018.01971 Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function Lydia-Ann J. Ghuneim1*, David L. Jones1, Peter N. Golyshin2 and Olga V. Golyshina2 1 School of Environment, Natural Resources and Geography, Bangor University, Bangor, United Kingdom, 2 School of Biological Sciences, Bangor University, Bangor, United Kingdom 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 mm 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 Edited by: Hongyue Dang, for a free-living lifestyle, making their survival reliant on other microbial community Xiamen University, China members. In these cases, the nano-sized prokaryotes can only be co-cultured with Reviewed by: their ‘hosts.’ This paper analyses the recent data on small-sized microorganisms in the Laura Steindler, University of Haifa, Israel context of their taxonomic diversity and potential functions in the environment. Konstantinos Ar. Kormas, Keywords: nano-sized microorganisms, ultramicrocells, filterable microorganisms, unculturable, oligotrophy, University of Thessaly, Greece copiotrophy Matthias Labrenz, Leibniz Institute for Baltic Sea Research (LG), Germany INTRODUCTION *Correspondence: Lydia-Ann J. Ghuneim Recent technological advances in microbiology have helped to reveal the enormous diversity of [email protected] prokaryotic life on our planet (Kuczynski et al., 2010; Caporaso et al., 2011; Thompson et al., 2017). Specialty section: While this has enabled us to characterize and map prokaryote populations across a diverse array of This article was submitted to ecosystems, the functional role of most of these organisms remains unknown, due to our inability Aquatic Microbiology, to culture, and study them in the laboratory. Nevertheless, using culture-independent approaches, a section of the journal e.g., metagenomics, many new candidate taxa that include nano-sized and filterable organisms have Frontiers in Microbiology been discovered. Received: 26 March 2018 Nano-sized microorganisms are termed ‘ultra-micro bacteria,’ ‘ultra-micro cells,’ ‘dwarf cells,’ Accepted: 06 August 2018 ‘ultra-small bacteria,’ ‘nanoorganisms,’ ‘nanobacteria,’ nanoarchaea and ‘nanobes’ (Velimirov, Published: 21 August 2018 2001; Baker et al., 2010; Duda et al., 2012). The term nanoarchaea only relates to the phylum Citation: Nanoarchaeota (Huber et al., 2002), although it is commonly erroneously used within the literature. Ghuneim L-AJ, Jones DL, The exact definition of these terms is widely debated and no clear set of guidelines currently Golyshin PN and Golyshina OV (2018) exists, however, it is considered that the microorganism must be in the “nano-range” (i.e., 50– Nano-Sized and Filterable Bacteria 400 nm) in size. It should also be noted that in regards to aquatic systems, these ultra-small-sized and Archaea: Biodiversity and Function. organisms are not part of nanoplankton (2.0–20 mm in size), but instead reside in the picoplankton Front. Microbiol. 9:1971. (0.2–2.0 mm) or femtoplankton (0.02–0.2 mm) communities (Sieburth et al., 1978; Fenchel, 1982; doi: 10.3389/fmicb.2018.01971 Azam et al., 1983). Frontiers in Microbiology| www.frontiersin.org 1 August 2018| Volume 9| Article 1971 fmicb-09-01971 August 18, 2018 Time: 18:55 # 2 Ghuneim et al. Nano-Sized and Filterable Prokaryotes Previous studies have focused on detection of ultra-small- 2012). Under this definition, nano-sized microorganisms are sized organisms in a wide range of environmental conditions associated with terms like ultra-small, ultramicro, nanoarchaea, including: acid mine drainage settings (AMD) (Baker and nanoforms, nanoorgansims, and nanobacteria (Schut et al., 1995; Banfield, 2003; Baker et al., 2006), glacial ice (Miteva and Kajander and Ciftcioglu, 1998; Velimirov, 2001; Huber et al., Brenchley, 2005), permafrost (Suzina et al., 2015), freshwater 2002; Miteva and Brenchley, 2005; Panikov, 2005; Comolli et al., (Fedotova et al., 2012; Ma et al., 2016; Nakai et al., 2016), 2009; Duda et al., 2012; Fedotova et al., 2012; Luef et al., 2015; subterranean bedrock (Wu et al., 2015), hypersaline lakes Giovannoni, 2017; Rogge et al., 2017). However, many standard- (Narasingarao et al., 2012), the open ocean (Venter et al., 2004; sized microorganisms (i.e., cell volumes > 0.1 mm3) also possess Giovannoni et al., 2005; Glaubitz et al., 2013; Rogge et al., small genomes (1.5–2.0 Mbp) and would therefore fall into the 2017), and the human body (Kajander and Ciftcioglu, 1998; ‘ultra-small’ category if based on these criteria alone. Kajander et al., 2003; He et al., 2015). The predictions from The third scenario are microorganisms that have the ability to genomic data from these environments suggest that there are pass through membrane filter pores with small diameters (0.45 or many microorganisms that contain small genomes and either are 0.22 mm) despite having larger cell sizes (above the dimensions present as free-living organisms or form a symbiotic relationship of 50–400 nm previously mentioned) (reviewed in Duda et al., with other life forms, which adds another level of complexity to 2012). This is often due to the absence of a rigid cell wall, assess their functional role in the environment. which allows these microorganisms to effectively squeeze through As the review of Duda et al.(2012) discusses a number small pores and as a result are commonly confused with nano- of issues related with ultramicrobacteria, the aim of present sized or ultramicro-sized. ‘Filterable’ microorganisms is the most review was to highlight the latest discoveries related to (1) appropriate term to define such microorganisms. taxonomic diversity, (2) biogeography, (3) current experimental In this review, a unified definition for nano-sized organisms approaches to characterize these organisms and (iv) potential role is proposed. We define them as microorganisms that exhibit of ultra-small Bacteria and Archaea within a contrasting range of constant dimensions of 50–400 nm (volume ≤ 0.1 mm3). environments. All microorganisms with synonymous names that fall under the definition provided are considered nano-sized organisms. Overview of Terminology Viruses and prions, which are smaller than 50 nm in size, When considering ultra-small or nano-sized organisms, it is are not considered to be living organisms (Figure 2 and important to note the significance of the terminology. There Table 1). In aquatic systems, nano-sized organisms are a part of is no singular definition of what a nano-sized organism is the picoplankton and femtoplankton communities, along with (ultra-small bacteria, ultra-micro bacteria, nanobes, nanoforms, viruses (Sieburth et al., 1978; Venter et al., 2004; Tringe et al., ultramicrocells, etc.) and consequently a variety of interpretations 2005; Salcher, 2014). exists. Many of the terms are either synonymous, as in the case of ultra-small and ultra-micro (Velimirov, 2001), or can be classified as separate organisms, as in the case of nanobacterium and MICROBIAL ADAPTATIONS nanobe (Duda et al., 2012). Here, we consider three scenarios for their denotation (Figure 1). In the natural environments microorganisms use an arsenal of The first scenario that these microorganisms originated from mechanisms
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