Bacterial Avidins Are a Widely Distributed Protein Family in Actinobacteria, Proteobacteria and Bacteroidetes Olli H

Laitinen et al. BMC Ecol Evo (2021) 21:53 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01784-y RESEARCH ARTICLE Open Access Bacterial avidins are a widely distributed protein family in Actinobacteria, Proteobacteria and Bacteroidetes Olli H. Laitinen1†, Tanja P. Kuusela1†, Sampo Kukkurainen1†, Anssi Nurminen1, Aki Sinkkonen2 and Vesa P. Hytönen1,3* Abstract Background: Avidins are biotin-binding proteins commonly found in the vertebrate eggs. In addition to streptavidin from Streptomyces avidinii, a growing number of avidins have been characterized from divergent bacterial species. However, a systematic research concerning their taxonomy and ecological role has never been done. We performed a search for avidin encoding genes among bacteria using available databases and classifed potential avidins according to taxonomy and the ecological niches utilized by host bacteria. Results: Numerous avidin-encoding genes were found in the phyla Actinobacteria and Proteobacteria. The diversity of protein sequences was high and several new variants of genes encoding biotin-binding avidins were found. The living strategies of bacteria hosting avidin encoding genes fall mainly into two categories. Human and animal patho- gens were overrepresented among the found bacteria carrying avidin genes. The other widespread category were bacteria that either fx nitrogen or live in root nodules/rhizospheres of plants hosting nitrogen-fxing bacteria. Conclusions: Bacterial avidins are a taxonomically and ecologically diverse group mainly found in Actinobacteria, Proteobacteria and Bacteroidetes, associated often with plant invasiveness. Avidin encoding genes in plasmids hint that avidins may be horizontally transferred. The current survey may be used as a basis in attempts to understand the ecological signifcance of biotin-binding capacity. Keywords: Avidin, Phylogeny, Biotin-binding, Defense protein, Plant invasiveness Background sites in each functional protein, and the existing methods Te frst known avidin was isolated from the chicken to biotinylate a vast variety of biomolecules, has made (Gallus gallus) egg white in 1941 [1] as a minor protein avidin an important biotechnological tool in protein component showing extremely high avidity to biotin (Kd purifcation, detection, and assay technologies, but also −15 ≈ 10 M) and is a text-book example of tight protein– in diagnostics and pharmaceuticals [3, 4]. ligand interaction [1, 2]. Tis combined with the avidin’s Te frst bacterial avidin, streptavidin, was isolated compact tetrameric structure with four biotin-binding from antibiotic-secreting Streptomyces avidinii bacteria in 1964 [5]. Since then, several new avidins have been experimentally verifed from both eukaryotic and *Correspondence: [email protected] prokaryotic species. Ten avidin family members were †Olli H. Laitinen, Tanja P. Kuusela and Sampo Kukkurainen contributed equally to this work. identifed in the chicken genome between the 1980s and 1 Faculty of Medicine and Health Technology, Tampere University, the early 2000s [6, 7], and they were showed to resemble Tampere, Finland avidin structurally and functionally when expressed as Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Laitinen et al. BMC Ecol Evo (2021) 21:53 Page 2 of 14 recombinant proteins [8, 9]. Further eukaryotic avidins and UniProtKB databases using verifed avidins as query have been found in other avian species, reptiles, amphib- sequences. We identifed 946 protein and 213 nucleo- ians, sea urchin, fsh, lancelet and fungi [10–12]. Several tide sequences corresponding to new putative avidins. In putative novel bacterial avidin genes have been detected addition, we identifed several new putative avidin clades, from bacteria in a wide variety of environmental niches each showing their characteristic sequence features. Fur- including symbiotic, marine, and pathogenic species. thermore, we inspected the genomic and habitational However, none of these bacterial avidins except strepta- context of the bacterial avidin family. Our results indicate vidin and closely related streptavidin v1 and v2 from that avidins are widespread among three bacterial phyla, Streptomyces venezuelae [13] have been confrmed to be and that the avidin-carrying bacteria inhabit several eco- expressed in nature. Avidins are made of beta barrels and logical niches and represent alternative lifestyles. Tis their oligomeric state vary from loose dimeric assembly study reveals avidin family being very rich and proposes to very stable tetramer. that avidin encoding genes are benefcial for bacteria in Avidin has been suggested to have antibiotic quali- various environments. ties, as it renders biotin vitamin unavailable. In ovipa- rous animals, avidins are theorized to protect the eggs Results from microbes [14]. Evidence that chicken oviductal tis- Avidins exist widely in bacteria sue produces avidin in response to bacterial, viral, and Queries were run against both protein and nucleotide environmental stress supports this hypothesis [14–17]. databases with a set of nine verifed avidin sequences. For A recent study revealed that avidin is expressed in avian the protein queries the amount of hits varied between primary gut epithelial cells along proinfammatory 285 and 303, while for the nucleotide queries the amount cytokines as acute phase proteins [18]. In line with these of hits varied between 13 and 182. As the pooled query fndings, two avidin genes, Bjavd 1 and 2 [19] were found results contained a high amount of redundancy, the pre- to be expressed in lancelet (Branchiostoma japonicum) in viously collected protein and nucleotide sequences were response to bacterial and heat shock stress. Interestingly, processed to obtain a cleaned-up set of unique 213 nucle- the Bjavd proteins appeared to recruit macrophages to otide and 946 protein sequences. Tis data together with the site of infection and thus acted as opsonins. While the set of verifed avidin sequences was used as a mate- avidin has not been found in plants, transgenic avidin- rial for later analyses. Based on bacterial species informa- expressing crops show resistance to insect pests [20, 21] tion gathered via BLAST searches, we made a systematic and a correlation between biotin availability and root analysis of bacterial genomes, and simplifed the list of feeding nematodes was found in legume rhizosphere avidins by selecting representative avidins among groups [22]. In fungi, the tamavidins (Tamavd 1 and Tamavd 2), of identical and highly similar proteins and associated discovered from the edible mushroom Pleurotus cornu- them to representative bacterial species. Tis group copiae, have been suggested to protect from phytopath- was supplemented in the revision phase with 14 protein ogenic fungi [23]. Simultaneously, biotin is essential sequences, including representing putative avidins from cofactor avidin expression may cause negative efects. Bacteroidetes. Tis resulted set of 118 diferent bacterial Known eukaryotic avidins are secreted proteins and species are shown in Additional fle 1: Table S1 and their this could be important factor to avoid the toxic efects. sequences are listed in FASTA format in Additional fle 2. Refecting the delicate balance in biotin availability, avidin-induced biotin defciency causes low hatching suc- Phylogeny, habitats, lifestyles and ecological signifcance cess and teratogenicity in birds and mice, refecting the of avidin harboring bacteria toxic nature of avidin [24]. Silencing of zebavidin expres- Those defined 118 bacterial species with putative avi- sion in zebrafsh larvae using morpholinos did not reveal dins belong mainly in phyla Proteobacteria, Actino- any signifcant changes in the early development of the bacteria and Bacteroidetes with a single hit in phylum fsh [25]. Terefore, despite all the eforts, the exact Synergistetes. In Actinobacteria, the most of the puta- biological role of avidins in various species is not fully tive avidins belong to different Streptomyces species understood. whereas in Proteobacteria the species are most often Although avidin genes have been found in several found within Xanthomonas, Rhizobium, Bradyrhizo- bacterial clades, no comprehensive phylogeny of bac- bium, Burkholderia, Legionella, Methylobacterium and terial avidin sequences has been done. In this study, we Mesorhizobium (Additional file 1: Table S1). Despite present a phylogeny of the

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