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Front. Microbiol. | doi: 10.3389/fmicb.2019.01198

Commentary: Manifold Routes to a Nucleus

 Christian Jogler1*, Sandra Wiegand1 and Damien P. Devos2
  • 1Radboud University Nijmegen, Netherlands
  • 2Centro Andaluz de Biología del Desarrollo (CABD), Spain

In the manuscript ‘Manifold Routes to a Nucleus’, Hendrickson and Poole question the assumption that the evolution of nuclear compartmentalization has been a singular event. They provide interesting observations on jumbophages and newly described archaea. However, their claim that bacteria from the Planctomycetes phylum display ‘nucleus-like compartmentation’ is based on an outdated interpretation of the planctomycetal cell plan (Fuerst and Sagulenko, 2011). Various comprehensive reviews on the paradigm shift in the field of planctomycetal research were recently published (Devos, 2014b;a;Rivas-Marin and Devos, 2018;Wiegand et al., 2018) and are summarized in Figure 1.

The concept of a nuclear structure outside the eukaryotes was introduced in 1991, when Fuerst and Webb postulated that the planctomycetal species Gemmata obscuriglobus harbors a bacterial ‘nucleus’ (Fuerst and Webb, 1991). At this time, Planctomycetes were thought to share similarities with bacteria and eukaryotes alike (Fig. 1, for review see (Fuerst and Sagulenko, 2011)). Besides the suggested nucleoid (Fuerst and Webb, 1991), the cytoplasm of Planctomycetes was considered to be compartmentalized by an intracytoplasmic membrane (Lindsay et al., 2001). In contrast to all other Gram-negative bacteria, Planctomycetes were believed to lack a peptidoglycan sacculus and their outermost (cytoplasmic) membrane was suggested to be surrounded by a proteinaceous cell wall instead (König et al., 1984;Liesack et al., 1986;Stackebrandt et al., 1986). Given this model of a planctomycetal cell (see Fig. 1A), it was not surprising that other typical eukaryotic hallmark-traits such as endocytosis (Fuerst and Sagulenko, 2010;Lonhienne et al., 2010) and separation of translation and transcription were suggested (Gottshall et al., 2014). Various interpretations were proposed, such as Planctomycetes are ‘beyond the bacterium’ (Fuerst and Sagulenko, 2011) or that they represent intermediate steps between pro- and eukaryotes (Devos and Reynaud, 2010).
However, the concept of the planctomycetal cell plane evolved (Fig. 1B). Others and we have found that Planctomycetes possess a peptidoglycan cell wall (Fig. 1C) (Jeske et al., 2015;van Teeseling et al., 2015) and the three-dimensional reconstruction of a G. obscuriglobus cell revealed interconnections of all previously suggested compartments, including the nucleus-like structure (Santarella-Mellwig et al., 2010). These finding of an interconnected tubulovesicular network - a continuous cytoplasm with invaginations of the cytoplasmic membrane (Acehan et al., 2013) - called for a reinterpretation of the classic cell plan (Devos, 2014b;a;Wiegand et al., 2018). We also investigated members of different phylogenetic branches of Planctomycetes in a comprehensive study involving mutagenesis and state-of-the-art microscopic techniques and demonstrated that canonical Planctomycetes are a variation of, but not an exception to, the Gram-negative cell plan (Devos, 2014b;a;Boedeker et al., 2017). Most importantly, all investigated planctomycetal species lack compartmentalization by additional membranes (Fig. 1D) (Boedeker et al., 2017). Consequently, there is no separate nucleus-like compartment in Planctomycetes. However, unusual large pores known as crateriform structures are found in the planctomycetal outer membrane (Fig. 1E) (König et al., 1984;Schlesner and Hirsch, 1984;Fuerst et al., 1991;Ward et al., 2006;Boedeker et al., 2017). Such structures are unique among bacteria and can be found on the surface of all Planctomycetes (Wiegand et al., 2018). We believe that these crateriform structures have been mistakenly interpreted as ‘nuclear pores’ in a recent study (Sagulenko et al., 2017). Despite these findings, alternative interpretations are still presented (Sagulenko et al., 2014;Feijoo-Siota et al., 2017).

However, we do acknowledge that one aspect of the potential planctomycetal ‘compartmentalization’ requires further investigation: one branch of the phylum, the one of the anammox bacteria, was shown to contain a separated subcellular compartment, the anammoxosome (Neumann et al., 2014). To obtain energy, ammonium is anaerobically oxidized to dinitrogen gas in this compartment whilst forming toxic hydrazine as intermediate metabolite (for review see (Peeters and van Niftrik, 2018)). Therefore, it was called the ‘bacterial mitochondrion’ (Jogler, 2014). Specific ladderane lipids were thought to protect the anammox membrane against leakage of hydrazine into the cytosol where it would harm the DNA (Sinninghe Damste et al., 2002). In their study, Hendrickson and Pool argue that this is an example for chemical protection of the DNA by an organelle. However, recently it was shown that ladderane membranes are as permeable to hydrazine as straight-chain lipid bilayers (Moss et al., 2018), representing a problem for, the authors’ hypothesis.

Regarding the main aspect of their article ‘Manifold Routes to a Nucleus’, Hendrickson and Poole unfortunately do not mention most of the above discussed research articles and others (Speth et al., 2012;Devos, 2014b;a;Rivas-Marin and Devos, 2018). By acknowledging that ‘the exact nature of this compartmentation is a matter of ongoing debate’ they neglect the fact that the described findings do not question the nature of the compartments but their very existence. This disregard leaves the reader under the impression that there is a bacterial nucleus. However, many of their suggestions suffer coherence when confronted with the most recent data.

Despite the absence of a nucleus-like structure, the phylum Planctomycetes and the extended PVC superphylum is still a relevant model for endomembrane formation - maybe related to DNA protection - and in any case for cell organization and complexity.

Keywords: nucleus, Compartmentation, planctomycetes, Nuclear Pore, evolution

Received: 09 Apr 2019; Accepted: 13 May 2019.

Edited by:

Ludmila Chistoserdova, University of Washington, United States

Reviewed by:

Svetlana N. Dedysh, Winogradsky Institute of Microbiology (RAS), Russia  

Copyright: © 2019 Jogler, Wiegand and Devos. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Christian Jogler, Radboud University Nijmegen, Nijmegen, Netherlands, christian@jogler.de