Utilization of Cobalamin is Ubiquitous in Early-Branching Fungal Phyla

Małgorzata Orłowska ,Kamil Steczkiewicz,Anna Muszewska

doi:10.2139/ssrn.3732362

Małgorzata Orłowska , Kamil Steczkiewicz + Show 1 more

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https://doi.org/10.2139/ssrn.3732362

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Abstract

Cobalamin is a cofactor present in essential metabolic pathways in animals and one of the water-soluble vitamins. It is a complex compound synthesized solely by prokaryotes. Cobalamin dependence is scattered across the tree of life. In particular, fungi and plants were deemed devoid of cobalamin. We demonstrate that cobalamin is utilized by all fungal lineages, except for Dikarya. This observation is supported by the genomic presence of both B12 dependent enzymes and cobalamin modifying enzymes. Moreover, the genes identified are actively transcribed in many taxa. Most fungal cobalamin dependent enzymes and cobalamin metabolism proteins are highly similar to their animal homologs. Phylogenetic analyses support a scenario of vertical inheritance of the cobalamin trait with several losses. Cobalamin usage was probably lost in Mucorinae and at the base of Dikarya which groups most of the model organisms which hindered B12-dependent metabolism discovery in fungi. Our results indicate that cobalamin dependence was a widely distributed trait at least in Opisthokonta, across diverse microbial eukaryotes and likely in the LECA.

Highlights

Cobalamin, known as vitamin B12, is the most common cobalt-containing compound in nature and one of eight known water-soluble vitamins grouped into B class
We looked for MetE which can substitute Methionine synthetase (MetH) (González et al 1996), RNR class I instead of class II (Jordan and Reichard 1998), and methylcitrate cycle (MCC) as an alternative to MM-CoA mutase pathway (Dubey et al 2013)
Our discoveries contradict the current opinion that fungi neither synthesize nor use cobalamin (Jah et al 2002; Duda, Pedziwilk, and Zodrow 1957) and do not have cobalt at all (Zhang, Ying, and Xu 2019). This claim remains true for Dikarya, but we demonstrate that the early diverging fungi do have proteins that either process or use cobalamin as a cofactor

Summary

Introduction

Known as vitamin B12, is the most common cobalt-containing compound in nature and one of eight known water-soluble vitamins grouped into B class. Seven enzymes from the above pathways seem to be uniquely present in B12-dependent organisms They either modify cobalamin or use it as a cofactor. The former group contains methylmalonyl Co-A mutaseassociated GTPase Cob (MeaB), cob(I)yrinic acid a,c-diamide adenosyltransferase (CblAdo. transferase), cyanocobalamin reductase (CblC), and cobalamin trafficking protein D (CblD) proteins, while the latter includes methionine synthase (MetH), methylmalonyl-CoA epimerase (MM-CoA epimerase) and methylmalonyl-CoA mutase (MM-CoA mutase) (Kräutler 2012). There is one more cobalamin-dependent enzyme that is present uniquely in archaebacteria, eubacteria, and bacteriophages This enzyme called ribonucleotide reductase class II (RNR class II) takes a part in DNA replication and repair ((Herrick and Sclavi 2007); (Larsson et al 2004)). We show that all B12dependent eukaryotic pathways are present in non-Dikarya fungi as well

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