Genomic analysis of Caldalkalibacillus thermarum TA2.A1 reveals aerobic alkaliphilic metabolism and evolutionary hallmar

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ORIGINAL PAPER

Genomic analysis of Caldalkalibacillus thermarum TA2.A1 reveals aerobic alkaliphilic metabolism and evolutionary hallmarks linking alkaliphilic bacteria and plant life Samuel I. de Jong1 · Marcel A. van den Broek1 · Alexander Y. Merkel2 · Pilar de la Torre Cortes1 · Falk Kalamorz3 · Gregory M. Cook4 · Mark C. M. van Loosdrecht1 · Duncan G. G. McMillan1  Received: 9 August 2020 / Accepted: 23 September 2020 © The Author(s) 2020

Abstract The aerobic thermoalkaliphile Caldalkalibacillus thermarum strain TA2.A1 is a member of a separate order of alkaliphilic bacteria closely related to the Bacillales order. Efforts to relate the genomic information of this evolutionary ancient organism to environmental adaptation have been thwarted by the inability to construct a complete genome. The existing draft genome is highly fragmented due to repetitive regions, and gaps between and over repetitive regions were unbridgeable. To address this, Oxford Nanopore Technology’s MinION allowed us to span these repeats through long reads, with over 6000-fold coverage. This resulted in a single 3.34 Mb circular chromosome. The profile of transporters and central metabolism gives insight into why the organism prefers glutamate over sucrose as carbon source. We propose that the deamination of glutamate allows alkalization of the immediate environment, an excellent example of how an extremophile modulates environmental conditions to suit its own requirements. Curiously, plant-like hallmark electron transfer enzymes and transporters are found throughout the genome, such as a cytochrome b6c1 complex and a C ­ O2-concentrating transporter. In addition, multiple self-splicing group II intron-encoded proteins closely aligning to those of a telomerase reverse transcriptase in Arabidopsis thaliana were revealed. Collectively, these features suggest an evolutionary relationship to plant life. Keywords  Genome · Alkaliphiles · Phylogeny · Evolution

Introduction

Communicated by A. Oren. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0079​2-020-01205​-w) contains supplementary material, which is available to authorized users. * Duncan G. G. McMillan [email protected] 1



Department of Biotechnology, Delft University of Technology, Delft, The Netherlands

2



Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Moscow, Russia

3

The New Zealand Institute for Plant and Food Research, Lincoln, New Zealand

4

Department of Microbiology and Immunology, The University of Otago, Dunedin, New Zealand



The alkaline world is a fascinating and geologically ancient environment (Horikoshi 2016). In line with this, Russell and Hall first theorized that life on earth might well have started in alkaline hot springs (Russell et al. 1988; Russell 2006), but whether this is true for all life is still a matter of intense debate (Miller and Bada 1988; Damer and Deamer 2015; Maruyama et al. 2019). Support for this theory appears to be ‘branch