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Hbtr, a Heterofunctional Homolog of the Virulence Regulator Tcpp, Facilitates the Transition Between Symbiotic and Planktonic Li

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Hbtr, a Heterofunctional Homolog of the Virulence Regulator Tcpp, Facilitates the Transition Between Symbiotic and Planktonic Li bioRxiv preprint doi: https://doi.org/10.1101/2020.03.31.019356; this version posted April 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 2 3 4 HbtR, a heterofunctional homolog of the virulence regulator TcpP, facilitates the 5 transition between symbiotic and planktonic lifestyles in Vibrio fischeri. 6 7 Brittany D. Bennett, Tara Essock-Burns, and Edward G. Ruby 8 9 Pacific Biosciences Research Center, University of Hawaiʻi—Manoa, Honolulu, HI 10 96813 11 12 Running head: Regulation of lifestyle transition in V. fischeri 13 14 Address correspondence: [email protected] 15 16 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.31.019356; this version posted April 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 17 Abstract 18 The bioluminescent bacterium Vibrio fischeri forms a mutually beneficial symbiosis with 19 the Hawaiian bobtail squid, Euprymna scolopes, in which the bacteria, housed inside a 20 specialized light organ, produce light used by the squid in its nocturnal activities. Upon 21 hatching, E. scolopes juveniles acquire V. fischeri from the seawater through a complex 22 process that requires, among other factors, chemotaxis by the bacteria along a gradient 23 of N-acetylated sugars into the crypts of the light organ, the niche in which the bacteria 24 reside. Once inside the light organ, V. fischeri transitions into a symbiotic, sessile state 25 in which the quorum-signaling regulator LitR induces luminescence. In this work we 26 show that expression of litR and luminescence are repressed by a homolog of the V. 27 cholerae virulence factor TcpP, which we have named HbtR. Further, we demonstrate 28 that LitR represses genes involved in motility and chemotaxis into the light organ and 29 activates genes required for exopolysaccharide production. 30 Importance 31 TcpP homologs are widespread throughout the Vibrio genus; however, the only protein 32 in this family described thus far is a V. cholerae virulence regulator. Here we show that 33 HbtR, the TcpP homolog in V. fischeri, has both a biological role and regulatory pathway 34 completely unlike that in V. cholerae. Through its repression of the quorum-signaling 35 regulator LitR, HbtR affects the expression of genes important for colonization of the E. 36 scolopes light organ. While LitR becomes activated within the crypts, and upregulates 37 luminescence and exopolysaccharide genes and downregulates chemotaxis and 38 motility genes, it appears that HbtR, upon expulsion of V. fischeri cells into seawater, 39 reverses this process to aid the switch from a symbiotic to a planktonic state. The bioRxiv preprint doi: https://doi.org/10.1101/2020.03.31.019356; this version posted April 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 40 possible importance of HbtR to the survival of V. fischeri outside of its animal host may 41 have broader implications for the ways in which bacteria transition between often vastly 42 different environmental niches. 43 44 Introduction 45 The Gram-negative bacterium Vibrio (Aliivibrio) fischeri is a model for the study of 46 biochemical processes underpinning bioluminescence, quorum sensing, and bacterial- 47 animal symbioses. Luminescence in V. fischeri is activated by a quorum-sensing 48 pathway that responds to high concentrations of two autoinducer molecules, N-(3- 49 oxohexanoyl)-L-homoserine lactone (3-oxo-C6-HSL (1)) and N-octanoyl-L-homoserine 50 lactone (C8-HSL (2)). When V. fischeri cells multiply to a certain density, C8-HSL and 3- 51 oxo-C6-HSL accumulate to high local concentrations, initiating a signaling cascade that 52 leads to upregulation of the regulator LuxR by the regulator LitR and consequent 53 activation of the luciferase operon, luxICDABEG (3–5); reviewed in (6). 54 Light production by V. fischeri is a crucial factor in the mutualistic symbiosis it 55 forms within the light organ of the Hawaiian bobtail squid, Euprymna scolopes (7–9). 56 Juvenile E. scolopes become colonized with V. fischeri shortly after hatching into 57 seawater containing this bacterium (10). V. fischeri cells initiate light-organ colonization 58 through a series of steps, including chemotaxis towards N-acetylated sugars released 59 by the squid (11, 12). After initial colonization of the squid light organ, the symbiosis 60 undergoes a daily cyclic rhythm of three basic stages for the remainder of the squid’s 61 life: during the day, V. fischeri cells grow to a high density in the crypts on carbon 62 sources provided by the squid (13, 14); at night, the bacteria produce light that aids in bioRxiv preprint doi: https://doi.org/10.1101/2020.03.31.019356; this version posted April 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 63 camouflage for the squid (15, 16); and at dawn, ~95% of the bacterial cells are expelled 64 from the light organ into the seawater, where they may initiate colonization of new squid 65 hatchlings, while the remaining ~5% repopulate the light organ (17, 18). 66 Previous work indicated that, in V. fischeri cells newly expelled from the light 67 organ, numerous genes are up- and downregulated relative to their level of expression 68 in planktonic cells (19). Two of the genes upregulated in expelled cells were VF_A0473 69 and VF_A0474, comprising a small operon annotated as encoding homologs of the 70 genetic regulator TcpP and its chaperone, TcpH. TcpP was first described in V. 71 cholerae as a virulence gene regulator (20, 21). During the early stages of V. cholerae 72 infection, TcpP works synergistically with another transcriptional regulator, ToxR, to 73 upregulate expression of the virulence regulator toxT and thereby activate expression of 74 cholera toxin and the toxin-coregulated pilus in response to changing environmental 75 conditions (21, 22). tcpPH expression is itself induced by AphA and AphB in response 76 to low oxygen or acidic pH (23–25). In V. cholerae El Tor biotypes, aphA expression is 77 repressed by HapR (the V. cholerae ortholog of LitR) upon initiation of quorum sensing 78 at high cell densities (26, 27). Additionally, activation of tcpPH expression by AphA and 79 AphB is inhibited by the global metabolic regulator Crp (28). This complex regulatory 80 pathway serves to upregulate tcpPH and, consequently, downstream virulence factors 81 under conditions consistent with entry into the vertebrate gut, a process reversed late in 82 the infection cycle before the bacteria exit the host and re-enter an aquatic environment 83 (29, 30). 84 No published genomes of V. fischeri strains encode homologs of either toxT or 85 cholera toxin genes. The genome of the model strain V. fischeri ES114 does encode bioRxiv preprint doi: https://doi.org/10.1101/2020.03.31.019356; this version posted April 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 86 annotated homologs of the toxin-coregulated pilus genes tcpFETSD and tcpCQBA, but 87 this strain is alone among the 66 currently available V. fischeri genomes to do so. The 88 V. fischeri genes regulated by the protein product of VF_A0473 are therefore unknown, 89 as are any upstream regulatory factors that determine under which conditions the 90 regulator is produced and active. Here we present evidence that VF_A0473 regulates 91 genes governing phenotypes relevant to the switch from symbiosis to a planktonic 92 lifestyle. We therefore rename VF_A0473 and VF_A0474, currently annotated as tcpP 93 and tcpH, as hbtR (habitat transition regulator) and hbtC (habitat transition chaperone). 94 In this work, we identify the HbtR regulon and uncover aspects of hbtRC regulation. 95 Further, we determine that LitR is repressed by HbtR and describe LitR-regulated 96 phenotypes beyond luminescence that are important for light-organ colonization. 97 98 Results 99 The HbtR regulon is distinct from that of TcpP. Considering that V. fischeri and V. 100 cholerae have significantly different lifestyles, as well as the absence in 65 of 66 101 sequenced V. fischeri genomes of homologs of virulence-factor genes regulated by 102 TcpP in V. cholerae, we postulated that HbtR has a distinct function from that of TcpP. 103 To determine the regulon of HbtR, RNA-seq was performed using ΔhbtRC mutant 104 strains of V. fischeri ES114 carrying either empty vector or an inducible vector with 105 hbtRC under control of the lac promoter. Notable among the RNA-seq results (Table S1 106 Excel file) is that none of the tcp pilus gene homologs encoded in the V. fischeri ES114 107 genome were expressed at significantly different levels in hbtRC strains carrying either bioRxiv preprint doi: https://doi.org/10.1101/2020.03.31.019356; this version posted April 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
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