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      Phyloproteomic and functional analyses do not support a split in the genus Borrelia (phylum Spirochaetes)

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          Abstract

          Background

          The evolutionary history of a species is frequently derived from molecular sequences, and the resulting phylogenetic trees do not include explicit functional information. Here, we aimed to assess the functional relationships among bacteria in the Spirochaetes phylum, based on the biological processes of 42,489 proteins in reference proteomes of 34 Spirochaetes species. We tested the hypothesis that the species in the genus Borrelia might be sufficiently different to warrant splitting them into two separate genera.

          Results

          A detrended canonical analysis demonstrated that the presence/absence of biological processes among selected bacteria contained a strong phylogenetic signal, which did not separate species of Borrelia. We examined the ten biological processes in which most proteins were involved consistently. This analysis demonstrated that species in Borrelia were more similar to each other than to free-life species ( Sediminispirochaeta, Spirochaeta, Sphaerochaeta) or to pathogenic species without vectors ( Leptospira, Treponema, Brachyspira), which are highly divergent. A dendrogram based on the presence/absence of proteins in the reference proteomes demonstrated that distances between species of the same genus among free-life or pathogenic non-vector species were higher than the distances between the 19 species (27 strains) of Borrelia. A phyloproteomic network supported the close functional association between species of Borrelia. In the proteome of 27 strains of Borrelia, only a few proteins had evolved separately, in the relapsing fever and Lyme borreliosis groups. The most prominent Borrelia proteins and processes were a subset of those also found in free-living and non-vectored pathogenic species. In addition, the functional innovation (i.e., unique biological processes or proteins) of Borrelia was very low, compared to other genera of Spirochaetes.

          Conclusions

          We found only marginal functional differences among Borrelia species. Phyloproteomic networks that included all pairwise combinations between species, proteins, and processes were more effective than other methods for evaluating the evolutionary relationships among taxa. With the limitations of data availability, our results did not support a split of the arthropod-transmitted spirochaetes into the proposed genera, Borrelia and Borreliella.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-019-1379-2) contains supplementary material, which is available to authorized users.

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          Most cited references 33

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          Fast unfolding of communities in large networks

          We propose a simple method to extract the community structure of large networks. Our method is a heuristic method that is based on modularity optimization. It is shown to outperform all other known community detection method in terms of computation time. Moreover, the quality of the communities detected is very good, as measured by the so-called modularity. This is shown first by identifying language communities in a Belgian mobile phone network of 2.6 million customers and by analyzing a web graph of 118 million nodes and more than one billion links. The accuracy of our algorithm is also verified on ad-hoc modular networks. .
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            Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution.

            Lateral gene transfer is an important mechanism of natural variation among prokaryotes, but the significance of its quantitative contribution to genome evolution is debated. Here, we report networks that capture both vertical and lateral components of evolutionary history among 539,723 genes distributed across 181 sequenced prokaryotic genomes. Partitioning of these networks by an eigenspectrum analysis identifies community structure in prokaryotic gene-sharing networks, the modules of which do not correspond to a strictly hierarchical prokaryotic classification. Our results indicate that, on average, at least 81 +/- 15% of the genes in each genome studied were involved in lateral gene transfer at some point in their history, even though they can be vertically inherited after acquisition, uncovering a substantial cumulative effect of lateral gene transfer on longer evolutionary time scales.
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              A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi.

              We have determined that Borrelia burgdorferi strain B31 MI carries 21 extrachromosomal DNA elements, the largest number known for any bacterium. Among these are 12 linear and nine circular plasmids, whose sequences total 610 694 bp. We report here the nucleotide sequence of three linear and seven circular plasmids (comprising 290 546 bp) in this infectious isolate. This completes the genome sequencing project for this organism; its genome size is 1 521 419 bp (plus about 2000 bp of undetermined telomeric sequences). Analysis of the sequence implies that there has been extensive and sometimes rather recent DNA rearrangement among a number of the linear plasmids. Many of these events appear to have been mediated by recombinational processes that formed duplications. These many regions of similarity are reflected in the fact that most plasmid genes are members of one of the genome's 161 paralogous gene families; 107 of these gene families, which vary in size from two to 41 members, contain at least one plasmid gene. These rearrangements appear to have contributed to a surprisingly large number of apparently non-functional pseudogenes, a very unusual feature for a prokaryotic genome. The presence of these damaged genes suggests that some of the plasmids may be in a period of rapid evolution. The sequence predicts 535 plasmid genes >/=300 bp in length that may be intact and 167 apparently mutationally damaged and/or unexpressed genes (pseudogenes). The large majority, over 90%, of genes on these plasmids have no convincing similarity to genes outside Borrelia, suggesting that they perform specialized functions.
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                Author and article information

                Contributors
                aestrada@unizar.es
                cabezasalejandrocruz@gmail.com
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                13 February 2019
                13 February 2019
                2019
                : 19
                Affiliations
                [1 ]Department of Animal Pathology, Faculty of Veterinary Medicine, Miguel Servet, 177, 50013 Zaragoza, Spain
                [2 ]ISNI 0000 0001 2149 7878, GRID grid.410511.0, UMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d’Alfort, , Université Paris-Est, ; 94700 Maisons-Alfort, France
                Article
                1379
                10.1186/s12862-019-1379-2
                6375133
                30760200
                cfe5bc4b-8b02-4bb9-8684-c78838632e7a
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: Diputación General de Aragón (DGA)
                Award ID: 218397
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Evolutionary Biology

                borrelia, borreliella, phyloproteomics, functional analysis, unsupported split

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