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Diversity in Natural Transformation Frequencies and Regulation Across Vibrio Species

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Diversity in Natural Transformation Frequencies and Regulation Across Vibrio Species bioRxiv preprint doi: https://doi.org/10.1101/683029; this version posted June 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 2 3 Diversity in natural transformation frequencies and regulation across Vibrio species 4 5 6 Chelsea A. Simpson1, Ram Podicheti2, Douglas B. Rusch2, Ankur B. Dalia1, Julia C. van 7 Kessel1* 8 9 10 1. Department of Biology, Indiana University, Bloomington, IN 47405 11 2. Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405 12 13 14 15 * Corresponding author: 16 Email: [email protected] 17 Telephone: 812-856-2235 18 Fax: 812-856-5710 19 20 Running title: Natural transformation in vibrios 21 22 Keywords: competence, natural transformation, vibrio 23 bioRxiv preprint doi: https://doi.org/10.1101/683029; this version posted June 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 Abstract 25 In marine Vibrio species, chitin-induced natural transformation enables bacteria to take up DNA 26 from the external environment and integrate it into their genome via homologous recombination. 27 Expression of the master competence regulator TfoX bypasses the need for chitin induction and 28 drives expression of the genes required for competence in several Vibrio species. Here, we 29 show that TfoX expression in two Vibrio campbellii strains, DS40M4 and NBRC 15631, enables 30 high frequencies of natural transformation. Conversely, transformation was not achieved in the 31 model quorum-sensing strain V. campbellii BB120 (previously classified as Vibrio harveyi). 32 Surprisingly, we find that quorum sensing is not required for transformation in V. campbellii 33 DS40M4. This result is in contrast to Vibrio cholerae that requires the quorum-sensing regulator 34 HapR to activate the competence regulator QstR. However, similar to V. cholerae, QstR is 35 necessary for transformation in DS40M4. To investigate the difference in transformation 36 frequencies between BB120 and DS40M4, we used previously studied V. cholerae competence 37 genes to inform a comparative genomics analysis coupled with transcriptomics. BB120 encodes 38 homologs of all known competence genes, but most of these genes were not induced by ectopic 39 expression of TfoX, which likely accounts for the non-functional natural transformation in this 40 strain. Comparison of transformation frequencies among Vibrio species indicates a wide 41 disparity among even closely related strains, with Vibrio vulnificus having the lowest functional 42 transformation frequency. We show that ectopic expression of both TfoX and QstR is sufficient 43 to produce a significant increase in transformation frequency in Vibrio vulnificus. 44 45 Significance 46 Naturally transformable or competent bacteria are able to take up DNA from their environment, 47 a key method of horizontal gene transfer for acquisition of new DNA sequences. Our research 48 shows that Vibrio species that inhabit marine environments exhibit a wide diversity in natural 49 transformation capability ranging from non-transformable to high transformation rates in which bioRxiv preprint doi: https://doi.org/10.1101/683029; this version posted June 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 50 10% of cells measurably incorporate new DNA. We show that the role of regulatory systems 51 controlling the expression of competence genes (e.g., quorum sensing) is conserved among 52 closely related species but differs throughout the genus. Expression of two key transcription 53 factors, TfoX and QstR, are necessary and sufficient to stimulate high levels of transformation in 54 Vibrio campbellii and recover low rates of transformation in Vibrio vulnificus. bioRxiv preprint doi: https://doi.org/10.1101/683029; this version posted June 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 55 Introduction 56 Natural transformation is a physiological state in which bacteria are able to take up 57 extracellular DNA from the environment, transport it across the cell envelope, and integrate it 58 into their genome via homologous recombination. In marine Vibrio species, competence is 59 induced by growth on the chitinous exoskeletons of crustaceans (1, 2). This process has been 60 best studied in Vibrio cholerae (reviewed in (2)). Insoluble polysaccharide chitin is broken down 61 by secreted extracellular chitinases (3). Soluble chitin oligosaccharides ultimately induce 62 expression of the master competence regulator TfoX (4), which activates expression of 63 numerous components of the competence machinery required to take up extracellular DNA. In 64 addition to the chitin-sensing system, V. cholerae cells must also have a functional quorum- 65 sensing system for natural transformation to be successful (1). Quorum sensing, the process of 66 cell-cell communication, allows bacterial cells to respond to changes in population density and 67 alter gene expression (5). The quorum-sensing systems in Vibrio species rely on detection of 68 extracellular autoinducers that are sensed by membrane-bound sensor kinases, which shuttle 69 phosphate to or away from the core response regulator LuxO at low cell density or high cell 70 density, respectively (5). At the end of this phosphorylation cascade at high cell density, the 71 master transcription factor called LuxR is activated, which controls expression of hundreds of 72 genes (6). LuxR is the name of the master transcription factor in Vibrio campbellii (previously 73 called Vibrio harveyi), whereas the homologs in other Vibrio species have different names: 74 HapR (V. cholerae), SmcR (Vibrio vulnificus), and OpaR (Vibrio parahaemolyticus) (7). In V. 75 cholerae, DhapR mutants are not competent, and this is due to HapR regulation of various 76 competence genes, including comEA, comEC, qstR, and dns (1, 8, 9). HapR directly activates 77 qstR (encoding a transcriptional regulator) and represses dns (encoding an extracellular DNase) 78 (8). QstR subsequently activates downstream genes required for DNA uptake and integration, 79 such as comEA, comEC, and comM (10). The requirement for HapR for competence can be 80 circumvented if qstR and tfoX expression are induced and the dns gene is deleted (10). bioRxiv preprint doi: https://doi.org/10.1101/683029; this version posted June 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 81 However, in wild-type V. cholerae, functional chitin-sensing and quorum-sensing systems are 82 required for competence. 83 Growth on chitin is sufficient to induce competence in several Vibrio species, including 84 V. cholerae, V. vulnificus, and V. parahaemolyticus (1, 11-13). Anecdotally, chitin-dependent 85 natural transformation has not been observed in other species. In these cases, it may be that 86 other environmental signals are required to induce competence or that laboratory conditions for 87 chitin sensing are not sufficient. Further, multiple studies have identified different transformation 88 capabilities among V. cholerae strains (14). However, because the chitin-sensing system drives 89 expression of the core competence regulator TfoX, overexpression of Tfox is sufficient to 90 bypass the requirement for chitin and induce competence in V. cholerae, V. vulnificus, V. 91 parahaemolyticus, and Vibrio natriegens (1, 12, 15-17). 92 The type strain of Vibrio campbellii called BB120 (or ATCC BAA-1116) is a model 93 system for studying quorum sensing in Vibrio species (18). This strain was historically called 94 Vibrio harveyi until a recent comparative genomics analysis reclassified it as V. campbellii (19). 95 However, while BB120 is highly studied, the competence of this strain and others in this species 96 was undetermined. Here, we show that the DS40M4 and NBRC 15631 environmental isolates 97 of V. campbellii are highly competent following TfoX overexpression, whereas the lab strain 98 BB120 and another environmental isolate called HY01 are not able to undergo natural 99 transformation either via chitin induction or TfoX overexpression. We compare multiple Vibrio 100 species and show that wide variation in transformation frequencies exists among strains in this 101 genus. 102 103 Results and Discussion 104 105 Induction of natural transformation via TfoX overexpression in V. campbellii DS4M04 and NBRC 106 15361 strains bioRxiv preprint doi: https://doi.org/10.1101/683029; this version posted June 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 107 Anecdotal reports and unpublished experiments have shown that the V. campbellii type 108 strain BB120 lacks the ability to undergo natural transformation. To formally test this, we 109 assayed for transformation of plasmid DNA into BB120 using both chitin-dependent and - 110 independent methods to induce competence (17, 20). For chitin-dependent transformations, 111 cells are incubated with powdered chitin from shrimp shells and DNA and plated with antibiotic 112
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