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Herbaspirillum Seropedicae Reveals a Potential New Emerging Bacterium Adapted to Human Hosts Helisson Faoro1,2,3* , Willian K

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Herbaspirillum Seropedicae Reveals a Potential New Emerging Bacterium Adapted to Human Hosts Helisson Faoro1,2,3* , Willian K Faoro et al. BMC Genomics (2019) 20:630 https://doi.org/10.1186/s12864-019-5982-9 RESEARCH ARTICLE Open Access Genome comparison between clinical and environmental strains of Herbaspirillum seropedicae reveals a potential new emerging bacterium adapted to human hosts Helisson Faoro1,2,3* , Willian K. Oliveira2,3, Vinicius A. Weiss1,2, Michelle Z. Tadra-Sfeir1, Rodrigo L. Cardoso1, Eduardo Balsanelli1, Liziane C. C. Brusamarello-Santos1, Doumit Camilios-Neto1,5, Leonardo M. Cruz1, Roberto T. Raittz2, Ana C. Q. Marques4, John LiPuma6, Cyntia M. T. Fadel-Picheth4, Emanuel M. Souza1 and Fabio O. Pedrosa1* Abstract Background: Herbaspirillum seropedicae is an environmental β-proteobacterium that is capable of promoting the growth of economically relevant plants through biological nitrogen fixation and phytohormone production. However, strains of H. seropedicae have been isolated from immunocompromised patients and associated with human infections and deaths. In this work, we sequenced the genomes of two clinical strains of H. seropedicae, AU14040 and AU13965, and compared them with the genomes of strains described as having an environmental origin. Results: Both genomes were closed, indicating a single circular chromosome; however, strain AU13965 also carried a plasmid of 42,977 bp, the first described in the genus Herbaspirillum. Genome comparison revealed that the clinical strains lost the gene sets related to biological nitrogen fixation (nif) and the type 3 secretion system (T3SS), which has been described to be essential for interactions with plants. Comparison of the pan-genomes of clinical and environmental strains revealed different sets of accessorial genes. However, antimicrobial resistance genes were found in the same proportion in all analyzed genomes. The clinical strains also acquired new genes and genomic islands that may be related to host interactions. Among the acquired islands was a cluster of genes related to lipopolysaccharide (LPS) biosynthesis. Although highly conserved in environmental strains, the LPS biosynthesis genes in the two clinical strains presented unique and non-orthologous genes within the genus Herbaspirillum. Furthermore, the AU14040 strain cluster contained the neuABC genes, which are responsible for sialic acid (Neu5Ac) biosynthesis, indicating that this bacterium could add it to its lipopolysaccharide. The Neu5Ac-linked LPS could increase the bacterial resilience in the host aiding in the evasion of the immune system. Conclusions: Our findings suggest that the lifestyle transition from environment to opportunist led to the loss and acquisition of specific genes allowing adaptations to colonize and survive in new hosts. It is possible that these substitutions may be the starting point for interactions with new hosts. Keywords: Herbaspirillum seropedicae, Clinical isolates, Genome comparison, Genomic adaptation, LPS substitution * Correspondence: [email protected]; [email protected]; [email protected] 1Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, Coronel Francisco H. dos Santos street, Curitiba, Paraná 81531-980, Brazil Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This 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. Faoro et al. BMC Genomics (2019) 20:630 Page 2 of 15 Background analysis as H. seropedicae (2 isolates), Herbaspirillum The genus Herbaspirillum belongs to the class β-Proteo- huttiense sp. putei (2 isolates), Herbaspirillum hut- bacteria and has 11 described species. These species tiense sp. huttiense (3 isolates), and Herbaspirillum were isolated from diverse environments such as water, frisingense (3 isolates). In addition, 18 isolates that contaminated soil, plant rhizosphere, plant internal tis- could not be classified were named lineages 1, 2 and sues and root nodules. The first described species of the 3[10]. Comparison of Herbaspirillum isolates recov- genus Herbaspirillum was the bacterium Herbaspirillum ered from environmental and clinical sources showed seropedicae, which was found colonizing the roots and no differences in adhesion capacity and cytotoxicity in aerial parts of important crops such as rice, sugarcane, human HeLa cells [11]. Although the above cases are maize and also tropical species such as pineapple and related to immunocompromised patients, Regunath et banana [1–3]. Since its isolation, this species has been al. described a case of bacteremia caused by gentami- verified as an endophytic non-pathogenic bacterium. It cin-resistant Herbaspirillum in an immunocompetent is able to promote plant growth through the production adult male farmer [12]. of phytohormones and by performing biological nitrogen Sequencing and comparison of genomes has been a fixation, a process through which diazotrophic bacteria powerful tool for phylogenetic studies and has helped convert atmospheric nitrogen (N2) to ammonium elucidate the different characteristics of environmental (NH4+)[4, 5]. Sequencing and analysis of the H. serope- and opportunistic (or pathogenic) bacteria within the dicae SmR1 genome allowed identification of the genes same taxonomic group [13, 14]. Thus, to better under- involved in nitrogen fixation (nif), genes related to ni- stand how these bacteria from the Herbaspirillum genus trate metabolism (nar, nas, nir), plant ethylene stress-re- are migrating from the environment to human hosts, we lieving 1-aminocyclopropane-1-carboxylate deaminase sequenced the genomes of two clinical isolates, identified (accD) and the plant-bacteria interaction type three se- as Herbaspirillum seropedicae AU14040 and Herbaspir- cretion system (T3SS) [6]. illum lineage 2 AU13965, isolated from cystic fibrosis pa- The first description of a Herbaspirillum genus bacter- tients by Spilker and collaborators [10]. We compared ium isolated from clinical samples occurred in 1996 [7]. these clinical isolate genomes with the genomes of envir- In this work, Baldani and coworkers analyzed the pheno- onmental isolates of H. seropedicae species and revealed types of 147 isolates and verified that a group of strains, gene losses and acquisitions that provide evidence for previously denominated as “group EF1”, belonged to the how strains of this species may evolve from plant endo- genus Herbaspirillum. However, the low degree of phytes to opportunistic human pathogens. DNA-DNA hybridization (~ 50%) did not allow for the identification of any of the Herbaspirillum species de- scribed at that time, and these strains were tentatively Results referred to as Herbaspirillum species 3 [7]. This group Genome assembly of bacteria was isolated from different types of human Genome assembly was performed through a hybrid samples, such as samples from wounds, urine, feces, strategy using data from different sequencing platforms, bacteremia, and gastritis as well as pulmonary, ocular different assembly programs and gap closure. The initial and pharyngeal infections. Since then, new species of the H. seropedicae AU14040 genome assembly had 52 con- genus Herbaspirillum have been associated with clinical tigs in 15 scaffolds. All internal gaps were closed after samples. Swantarat et al. reported the first fatal case-re- the first round of gap closure remaining 15 contigs. lated H. seropedicae infection: a case of bacteremia sec- These 15 contigs were ordinated in the SmR1 reference ondary to pneumonia in a 65-year-old man with end- genome using nucmer, yielding 1 scaffold. After the sec- stage renal disease and multiple myeloma [8]. Chem- ond round of gap closure, 4 gaps remained in the gen- ically et al. (2015) reported a study conducted at the ome that corresponded to repeat regions and rRNA University of Texas MD Anderson Cancer Center in operons and were resolved individually using blastn and which cases of patients with sepsis, whose infectious FGAP. After read mapping in the assembled genome, no agents were previously classified as Burkholderia sp., regions of zero coverage or structural inconsistencies were actually bacteria of the genus Herbaspirillum [9]. A were found. The genome sequence of H. seropedicae similar case was described at the University of Michigan AU14040 was deposited in the NCBI database under ac- Pediatric Hospital where a reanalysis indicated that of 1, cession number CP013136. The complete genome se- 100 bacteria isolated from the sputum samples of pa- quence of H. seropedicae AU14040 has 5,418,688 bp in a tients with cystic fibrosis, previously classified as Bur- single circular DNA molecule with a GC% content of kholderia sp., approximately 3% (28 isolates) were from 63.1%. The coding sequences cover 88.3% of the genome the Herbaspirillum genus [10]. The isolates from this and are distributed in 4,887 predicted protein-coding re- study were classified by 16S rRNA gene sequence gions, 3 complete rRNA operons and 57 tRNA genes. Faoro et al. BMC Genomics (2019) 20:630 Page 3 of 15 The initial assembly of the Herbaspirillum lineage 2 Phylogenetic classification
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