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Thalassoglobus Polymorphus Sp. Nov., a Novel Planctomycete Isolated Close to a Public Beach of Mallorca Island

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Thalassoglobus Polymorphus Sp. Nov., a Novel Planctomycete Isolated Close to a Public Beach of Mallorca Island Antonie van Leeuwenhoek https://doi.org/10.1007/s10482-020-01437-y (0123456789().,-volV)( 0123456789().,-volV) ORIGINAL PAPER Thalassoglobus polymorphus sp. nov., a novel Planctomycete isolated close to a public beach of Mallorca Island Elena Rivas-Marin . Sandra Wiegand . Nicolai Kallscheuer . Mareike Jogler . Stijn H. Peeters . Anja Heuer . Mike S. M. Jetten . Christian Boedeker . Manfred Rohde . Damien P. Devos . Christian Jogler Received: 31 March 2020 / Accepted: 11 June 2020 Ó The Author(s) 2020 Abstract Access to axenic cultures is crucial to optimal growth at pH 7.0–7.5 and 30 °C and exhibits extend the knowledge of the biology, lifestyle or typical features of Planctomycetes. Cells of the strain metabolic capabilities of bacteria from different phyla. are spherical to pear-shaped, divide by polar budding The phylum Planctomycetes is an excellent example with daughter cells showing the same shape as the since its members display an unusual cell biology and mother cell, tend to aggregate, display a stalk and complex lifestyles. As a contribution to the current produce matrix or fimbriae. Strain Mal48T showed collection of axenic planctomycete cultures, here we 95.8% 16S rRNA gene sequence similarity with the describe strain Mal48T isolated from phytoplankton recently described Thalassoglobus neptunius material sampled at the coast of S’Arenal close to KOR42T. The genome sequence of the novel isolate Palma de Mallorca (Spain). The isolated strain shows has a size of 6,357,355 bp with a G?C content of 50.3%. A total of 4874 protein-coding genes, 41 tRNA genes and 2 copies of the 16S rRNA gene are encoded E. Rivas-Marin Á D. P. Devos in the genome. Based on phylogenetic, morphological Centro Andaluz de Biologı´a del Desarrollo, CSIC, Universidad Pablo de Olavide, Seville, Spain and physiological analyses, we conclude that strain Mal48T (= DSM 100737T = LMG 29019T) should be S. Wiegand classified as the type strain of a new species in the Institute for Biological Interfaces 5, Karlsruhe Institute of genus Thalassoglobus, for which the name Thalas- Technology, Eggenstein-Leopoldshafen, Germany soglobus polymorphus sp. nov. is proposed. S. Wiegand Á N. Kallscheuer Á S. H. Peeters Á M. S. M. Jetten Á C. Jogler Keywords Marine bacteria Á PVC superphylum Á Department of Microbiology, Radboud Universiteit, Mallorca coast Á Planctomicrobium piriforme Á Nijmegen, The Netherlands Thalassoglobus neptunius M. Jogler Á C. Jogler (&) Department of Microbial Interactions, Friedrich-Schiller University, Jena, Germany e-mail: [email protected] Introduction A. Heuer Á C. Boedeker Leibniz Institute DSMZ, Brunswick, Germany The phylum Planctomycetes forms the medically, environmentally and biotechnologically important M. Rohde Central Facility for Microscopy, Helmholtz Centre for PVC superphylum together with Verrucomicrobia, Infection Research, Brunswick, Germany Lentisphaerae, Kirimatiellaeota and Chlamydiae 123 Antonie van Leeuwenhoek (Wagner and Horn 2006; Devos and Ward 2014; envelope architecture. Some strains have been shown Wiegand et al. 2018). Planctomycetes are ubiquitous to have expanded cytoplasmic membranes, a different bacteria, which colonise a variety of environments composition of peptidoglycan or condensed DNA, but from terrestrial to aquatic, marine or freshwater, in all of these characteristics are variations rather than which they act as important contributors to the activity exceptions to the Gram-negative cell plan (Devos of the global carbon and nitrogen cycle (Wiegand et al. 2014a, b; Boedeker et al. 2017; Rivas-Marı´n and 2020). One example of such an activity includes Devos 2018). members of the class Candidatus Brocadiae capable of Although most of the controversies have been performing anaerobic ammonium oxidation (anam- resolved, the prospect of deciphering of the molecular mox) (Strous et al. 1999). The anammox process is and cellular biology of Planctomycetes is still very industrially exploited for removal of ammonia during exciting. Several of their peculiarities need to be wastewater treatment (Peeters and van Niftrik 2019). studied in depth. This is e.g. the case for their unusual Members of the classes Phycisphaerae and Plancto- mechanism of proliferation. Members of the class mycetia are frequently found attached to algal surfaces. Phycisphaerae typically divide by binary fission, Both, cultivation-dependent and -independent meth- while species within the class Planctomycetia divide ods, have proven the frequent association of Plancto- by budding. It has been also reported that related mycetes with macroalgae (Bengtsson and Øvrea˚s members of the proposed phylum ‘Saltotorellota’ are 2010; Bondoso et al. 2014, 2017; Lage and Bondoso capable of switching between both mechanisms 2014). The ability to attach to surfaces is prerequisite (Wiegand et al. 2019). Surprisingly, all Plancto- for biofilm formation on biotic and abiotic surfaces mycetes lack the canonical divisome protein FtsZ as (Bengtsson and Øvrea˚s 2010; Kohn et al. 2020a, b). well as some other ‘essential’ division proteins Furthermore, the genomes of Planctomycetes code for (Pilhofer et al. 2008; Rivas-Marı´n et al. 2016a; enzymes putatively involved in the degradation of Rivas-Marin et al. 2020). Their complex endomem- complex carbon substrates (Wecker et al. 2009; brane systems and their uncommon capacity to take up Wegner et al. 2013). This might be a decisive macromolecules are also subject of current studies advantage in competitive environments since such (Boedeker et al. 2017). Planctomycetes appear to be compounds are one of the few sources of carbon and resistant to many antibiotics (Cayrou et al. 2010; energy in the otherwise oligotrophic seawater (Lachnit Godinho et al. 2019) and their estimated capacity to et al. 2013; Jeske et al. 2013; Kim et al. 2016). produce secondary metabolites is quite high (Jeske Historically, Planctomycetes were thought to dis- et al. 2013, 2016). This assumption is based on the play a number of exceptional traits. Amongst others, a presence of secondary metabolite-related gene clus- compartmentalised cell plan, a nucleus-like structure ters and the activity of small molecules produced and and the lack of peptidoglycan were proposed (Ko¨nig experimentally tested (Calisto et al. 2019; Grac¸a et al. et al. 1984; Fuerst and Webb 1991; Lindsay et al. 2016; Jeske et al. 2016; Panter et al. 2019; Wiegand 1997; Lonhienne et al. 2010). Due to the emergence of et al. 2020). more sophisticated microscopic techniques and In this study, we describe a novel strain, Mal48T, genetic tools allowing genetic modification of Planc- which was isolated from phytoplankton sampled in the tomycetes, these misinterpretations have been Mediterranean Sea close to Palma de Mallorca resolved (Jogler et al. 2011; Rivas-Marı´n et al. (Spain). Based on the results obtained, we conclude 2016b). Peptidoglycan has been detected in several that strain Mal48T represents a novel species of the members of the phylum (Jeske et al. 2015; van recently described genus Thalassoglobus within the Teeseling et al. 2015) and their internal compartments family Planctomycetaceae (Kohn et al. 2020a). were found to be invaginations of the cytoplasmic membrane (Santarella-Mellwig et al. 2013; Acehan et al. 2014; Boedeker et al. 2017), with the exception Materials and methods of the anammoxosome of members of the class Candidatus Brocadiae (Niftrik et al. 2006). It is now Cultivation conditions and isolation Strain Mal48T well accepted that Planctomycetes is a peculiar was isolated on the 23th of September 2014 from phylum of bacteria featuring a diderm bacterial cell phytoplankton collected at the coast of S’Arenal close 123 Antonie van Leeuwenhoek to Palma de Mallorca (Spain) (sampling location: Kallscheuer et al. 2019a; Dedysh et al. 2020). SINA 39.5126 N 2.7470 E). After centrifugation of the was used to perform the 16S rRNA gene sequence sampling material, the pellet was resuspended in alignment (Pruesse et al. 2012). The phylogenetic 100 lL sterile artificial seawater (ASW) and streaked inference was performed employing a maximum on a plate containing M1H medium with N-acetylglu- likelihood approach with 1000 bootstraps, the nucleo- cosamine (NAG) and ASW (designated M1H NAG tide substitution model GTR, gamma distribution and ASW) (Kallscheuer et al. 2019a) solidified with 15 g/ estimation of proportion of invariable sites L agar and additionally supplemented with 200 mg/L (GTRGAMMAI option) (Stamatakis 2014). Three ampicillin, 500 mg/L streptomycin and 20 mg/L 16S rRNA genes from members of the PVC super- cycloheximide. Plates were incubated at 28 °C for phylum, but outside of the phylum Planctomycetes, 3–4 weeks and isolated colonies were then streaked on were used as outgroup (Opitutus terrae, acc. No. fresh M1H NAG ASW plates. Initial amplification and AJ229235; Kiritimatiella glycovorans, acc. no. sequencing of the 16S rRNA gene was performed as NR_146840 and Lentisphaera araneosa, acc. no. previously described (Rast et al. 2017). This step was NR_027571). The average nucleotide identity (ANI) included to ensure that the isolated strain is indeed a was calculated using OrthoANI (Lee et al. 2016) and member of the phylum Planctomycetes. the average amino acid identity (AAI) was gained Physiological analyses For temperature and pH using the aai.rb script of the enveomics collection optima determination M1H NAG ASW medium was (Rodriguez-R and Konstantinidis 2016). The percent- used. The strain was cultivated at pH 8 at different age of conserved
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