Chapter 19 : Caroline Harwood: With Grace, Enthusiasm, and True Grit

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Caroline Harwood is a microbiologist working to decipher pathways of biodegradation, signal transduction, and biofuel exploration at the biochemical and molecular levels. In addition to her research career, she is also an excellent writer and mentor whose enthusiasm for sciences fosters a truly collaborative atmosphere. This chapter by Rebecca E. Parales and Margaret McFall-Ngai covers Dr. Harwood’s career and personal reflections from the authors as well as a number of her mentees from over the years.

Citation: Parales R, McFall-Ngai M. 2018. Caroline Harwood: With Grace, Enthusiasm, and True Grit, p 171-182. In Whitaker R, Barton H (ed), Women in Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555819545.ch19
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Carrie Harwood, with her signature enthusiastic smile.

Citation: Parales R, McFall-Ngai M. 2018. Caroline Harwood: With Grace, Enthusiasm, and True Grit, p 171-182. In Whitaker R, Barton H (ed), Women in Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555819545.ch19
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1. Harwood CS,, Canale-Parola E . 1981. Branched-chain amino acid fermentation by a marine spirochete: strategy for starvation survival. J Bacteriol 148 : 109 116.
2. Harwood CS,, Canale-Parola E . 1981. Adenosine 5′-triphosphate-yielding pathways of branched-chain amino acid fermentation by a marine spirochete. J Bacteriol 148 : 117 123.
3. Harwood CS,, Canale-Parola E . 1982. Properties of acetate kinase isozymes and a branched-chain fatty acid kinase from a spirochete. J Bacteriol 152 : 246 254.
4. Harwood CS,, Jannasch HW,, Canale-Parola E . 1982. Anaerobic spirochete from a deep-sea hydrothermal vent. Appl Environ Microbiol 44 : 234 237.
5. Harwood CS,, Canale-Parola E . 1983. Spirochaeta isovalercia sp. nov., a marine anaerobe that forms branched-chain fatty acids as fermentation products. Int J Syst Bacteriol 33 : 573 579.
6. Harwood CS,, Rivelli M,, Ornston LN . 1984. Aromatic acids are chemoattractants for Pseudomonas putida. J Bacteriol 160 : 622 628.
7. Harwood CS,, Ornston LN . 1984. TOL plasmid can prevent induction of chemotactic responses to aromatic acids. J Bacteriol 160 : 797 800.
8. Harwood CS,, Parales RE,, Dispensa M . 1990. Chemotaxis of Pseudomonas putida toward chlorinated benzoates. Appl Environ Microbiol 56 : 1501 1503.
9. Harwood CS,, Nichols NN,, Kim M-K,, Ditty JL,, Parales RE . 1994. Identification of the pcaRKF gene cluster from Pseudomonas putida: involvement in chemotaxis, biodegradation, and transport of 4-hydroxybenzoate. J Bacteriol 176 : 6479 6488.
10. Grimm AC,, Harwood CS . 1997. Chemotaxis of Pseudomonas spp. to the polyaromatic hydrocarbon naphthalene. Appl Environ Microbiol 63 : 4111 4115.
11. Grimm AC,, Harwood CS . 1999. NahY, a catabolic plasmid-encoded receptor required for chemotaxis of Pseudomonas putida to the aromatic hydrocarbon naphthalene. J Bacteriol 181 : 3310 3316.
12. Parales RE,, Ditty JL,, Harwood CS . 2000. Toluene-degrading bacteria are chemotactic towards the environmental pollutants benzene, toluene, and trichloroethylene. Appl Environ Microbiol 66 : 4098 4104.
13. Hawkins AC,, Harwood CS . 2002. Chemotaxis of Ralstonia eutropha JMP134(pJP4) to the herbicide 2,4-dichlorophenoxyacetate. Appl Environ Microbiol 68 : 968 972.
14. Ditty JL,, Grimm AC,, Harwood CS . 1998. Identification of a chemotaxis gene region from Pseudomonas putida. FEMS Microbiol Lett 159 : 267 273.
15. Ditty JL,, Harwood CS . 1999. Conserved cytoplasmic loops are important for both the transport and chemotaxis functions of PcaK, a protein from Pseudomonas putida with 12 membrane-spanning regions. J Bacteriol 181 : 5068 5074.
16. Nichols NN,, Harwood CS . 2000. An aerotaxis transducer gene from Pseudomonas putida. FEMS Microbiol Lett 182 : 177 183.
17. Ferrández A,, Hawkins AC,, Summerfield DT,, Harwood CS . 2002. Cluster II che genes from Pseudomonas aeruginosa are required for an optimal chemotactic response. J Bacteriol 184 : 4374 4383.
18. Ditty JL,, Harwood CS . 2002. Charged amino acids conserved in the aromatic acid/H + symporter family of permeases are required for 4-hydroxybenzoate transport by PcaK from Pseudomonas putida. J Bacteriol 184 : 1444 1448.
19. Hickman JW,, Tifrea DF,, Harwood CS . 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102 : 14422 14427.
20. Güvener ZT,, Harwood CS . 2007. Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66 : 1459 1473.
21. Hickman JW,, Harwood CS . 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69 : 376 389.
22. Baraquet C,, Murakami K,, Parsek MR,, Harwood CS . 2012. The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res 40 : 7207 7218.
23. O’Connor JR,, Kuwada NJ,, Huangyutitham V,, Wiggins PA,, Harwood CS . 2012. Surface sensing and lateral subcellular localization of WspA, the receptor in a chemosensory-like system leading to c-di-GMP production. Mol Microbiol 86 : 720 729.
24. Huangyutitham V,, Güvener ZT,, Harwood CS . 2013. Subcellular clustering of the phosphorylated WspR response regulator protein stimulates its diguanylate cyclase activity. mBio 4 : e00242-13.
25. Irie Y,, Borlee BR,, O’Connor JR,, Hill PJ,, Harwood CS,, Wozniak DJ,, Parsek MR . 2012. Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 109 : 20632 20636.
26. Baraquet C,, Harwood CS . 2013. C-di-GMP represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer binding protein FleQ. Proc Natl Acad Sci U S A 110 : 18478 18483.
27. Baraquet C,, Harwood CS . 2015. A FleQ DNA binding consensus sequence revealed by studies of FleQ-dependent regulation of biofilm gene expression in Pseudomonas aeruginosa. J Bacteriol 198 : 178 186.
28. Matsuyama BY,, Krasteva PV,, Baraquet C,, Harwood CS,, Sondermann H,, Navarro MV . 2016. Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 113 : E209 E218.
29. Geissler JF,, Harwood CS,, Gibson J . 1988. Purification and properties of benzoate-coenzyme A ligase, a Rhodopseudomonas palustris enzyme involved in the anaerobic degradation of benzoate. J Bacteriol 170 : 1709 1714.
30. Merkel SM,, Eberhard AE,, Gibson J,, Harwood CS . 1989. Involvement of coenzyme A thioesters in anaerobic metabolism of 4-hydroxybenzoate by Rhodopseudomonas palustris. J Bacteriol 171 : 1 7.
31. Gibson J,, Dispensa M,, Fogg GC,, Evans DT,, Harwood CS . 1994. 4-Hydroxybenzoate-coenzyme A ligase from Rhodopseudomonas palustris: purification, gene sequence, and role in anaerobic degradation. J Bacteriol 176 : 634 641.
32. Kim M-K,, Harwood CS . 1991. Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Microbiol Lett 83 : 199 204.
33. Dispensa M,, Thomas CT,, Kim M-K,, Perrotta JA,, Gibson J,, Harwood CS . 1992. Anaerobic growth of Rhodopseudomonas palustris on 4-hydroxybenzoate is dependent on AadR, a member of the cyclic AMP receptor protein family of transcriptional regulators. J Bacteriol 174 : 5803 5813.
34. Perrotta JA,, Harwood CS . 1994. Anaerobic metabolism of cyclohex-1-ene-1-carboxylate, a proposed intermediate of benzoate degradation by Rhodopseudomonas palustris. Appl Environ Microbiol 60 : 1775 1782.
35. Egland PG,, Pelletier DA,, Dispensa M,, Gibson J,, Harwood CS . 1997. A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc Natl Acad Sci U S A 94 : 6484 6489.
36. Gibson J,, Dispensa M,, Harwood CS . 1997. 4-Hydroxybenzoyl-CoA reductase (dehydroxylating) is required for anaerobic degradation of 4-hydroxybenzoate by Rhodopseudomonas palustris and shares features with molybdenum-containing hydroxylases. J Bacteriol 179 : 301 309.
37. Egland PG,, Gibson J,, Harwood CS . 1995. Benzoate-coenzyme A ligase, encoded by badA, is one of three ligases able to catalyze benzoyl-coenzyme A formation during anaerobic growth of Rhodopseudomonas palustris on benzoate. J Bacteriol 177 : 6545 6551.
38. Egland PG,, Harwood CS . 1999. BadR, a new MarR family member, regulates anaerobic benzoate degradation by Rhodopseudomonas palustris in concert with AadR, an Fnr family member. J Bacteriol 181 : 2102 2109.
39. Pelletier DA,, Harwood CS . 1998. 2-Ketocyclohexanecarboxyl coenzyme A hydrolase, the ring cleavage enzyme required for anaerobic benzoate degradation by Rhodopseudomonas palustris. J Bacteriol 180 : 2330 2336.
40. Egland PG,, Harwood CS . 2000. HbaR, a 4-hydroxybenzoate sensor and FNR-CRP superfamily member, regulates anaerobic 4-hydroxybenzoate degradation by Rhodopseudomonas palustris. J Bacteriol 182 : 100 106.
41. Pelletier DA,, Harwood CS . 2000. 2-Hydroxycyclohexanecarboxyl coenzyme A dehydrogenase, an enzyme characteristic of the anaerobic benzoate degradation pathway used by Rhodopseudomonas palustris. J Bacteriol 182 : 2753 2760.
42. Harrison FH,, Harwood CS . 2005. The p imFABCDE operon from Rhodopseudomonas palustris mediates dicarboxylic acid degradation and participates in anaerobic benzoate degradation. Microbiology 151 : 727 736.
43. Peres CM,, Harwood CS . 2006. BadM is a transcriptional repressor and one of three regulators that control benzoyl coenzyme A reductase gene expression in Rhodopseudomonas palustris. J Bacteriol 188 : 8662 8665.
44. Crosby HA,, Heiniger EK,, Harwood CS,, Escalante-Semerana JC . 2010. Reversible N-lysine acetylation regulates the activity of acyl-CoA synthetases involved in anaerobic benzoate catabolism in Rhodopseudomonas palustris. Mol Microbiol 75 : 1007 1020.
45. Larimer FW,, Chain P,, Hauser L,, Lamerdin J,, Malfatti S,, Do L,, Land ML,, Pelletier DA,, Beatty JT,, Lang AS,, Tabita FR,, Gibson JL,, Hanson TE,, Bobst C,, Torres JL,, Peres C,, Harrison FH,, Gibson J,, Harwood CS . 2004. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22 : 55 61.
46. Oda Y,, Larimer FW,, Chain PS,, Malfatti S,, Shin MV,, Vergez LM,, Hauser L,, Land ML,, Braatsch S,, Beatty JT,, Pelletier DA,, Schaefer AL,, Harwood CS . 2008. Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. Proc Natl Acad Sci U S A 105 : 18543 18548.
47. Oda Y,, Samanta SK,, Rey F,, Wu L,, Liu X-D,, Yan T-F,, Zhou J,, Harwood CS . 2005. Functional genomic analysis of three nitrogenase isozymes in Rhodopseudomonas palustris. J Bacteriol 187 : 7784 7794.
48. Rey FE,, Oda Y,, Harwood CS . 2006. Regulation of uptake hydrogenase and effects of hydrogen utilization on gene expression in Rhodopseudomonas palustris. J Bacteriol 188 : 6143 6152.
49. Rey FE,, Heiniger EK,, Harwood CS . 2007. Redirection of metabolism for biological hydrogen production. Appl Environ Microbiol 73 : 1665 1671.
50. Gosse JL,, Engel BJ,, Rey FE,, Harwood CS,, Scriven LE,, Flickinger MC . 2007. Hydrogen production by photoreactive nanoporous latex coatings of nongrowing Rhodopseudomonas palustris CGA009. Biotechnol Prog 23 : 124 130.
51. Huang JJ,, Heiniger EK,, McKinlay JB,, Harwood CS . 2010. Production of hydrogen gas from light and the inorganic electron donor thiosulfate by Rhodopseudomonas palustris. Appl Environ Microbiol 76 : 7717 7722.
52. Gosse JL,, Engel BJ,, Hui JC,, Harwood CS,, Flickinger MC . 2010. Progress toward a biomimetic leaf: 4,000 h of hydrogen production by coating-stabilized nongrowing photosynthetic Rhodopseudomonas palustris. Biotechnol Prog 26 : 907 918.
53. Heiniger EK,, Oda Y,, Samanta SK,, Harwood CS . 2012. How posttranslational modification of nitrogenase is circumvented in Rhodopseudomonas palustris strains that produce hydrogen gas constitutively. Appl Environ Microbiol 78 : 1023 1032.
54. Adessi A,, McKinlay JB,, Harwood CS,, DePhilippis R . 2012. A Rhodopseudomonas palustris nifA* mutant produces H 2 from NH 4 +-containing vegetable wastes. Int J Hydrogen Energy 37 : 15893 15900.
55. McKinlay JB,, Oda Y,, Rühl M,, Posto AL,, Sauer U,, Harwood CS . 2014. Non-growing Rhodopseudomonas palustris increases the hydrogen gas yield from acetate by shifting from the glyoxylate shunt to the tricarboxylic acid cycle. J Biol Chem 289 : 1960 1970.
56. Schaefer AL,, Greenberg EP,, Oliver CM,, Oda Y,, Huang JJ,, Bittan-Banin G,, Peres CM,, Schmidt S,, Juhaszova K,, Sufrin JR,, Harwood CS . 2008. A new class of homoserine lactone quorum-sensing signals. Nature 454 : 595 599.
57. Hirakawa H,, Oda Y,, Phattarasukol S,, Armour CD,, Castle JC,, Raymond CK,, Lappala CR,, Schaefer AL,, Harwood CS,, Greenberg EP . 2011. Activity of the Rhodopseudomonas palustris p-coumaroyl-homoserine lactone-responsive transcription factor RpaR. J Bacteriol 193 : 2598 2607.
58. Lindemann A,, Pessi G,, Schaefer AL,, Mattmann ME,, Christensen QH,, Kessler A,, Hennecke H,, Blackwell HE,, Greenberg EP,, Harwood CS . 2011. Quorum sensing in the soybean root-nodulating bacterium Bradyrhizobium japonicum: identification of isovaleryl-homoserine lactone, an unusual branched-chain signal. Proc Natl Acad Sci U S A 108 : 16750 16770.
59. Ahlgren NA,, Harwood CS,, Schaefer AL,, Giraud E,, Greenberg EP . 2011. Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia. Proc Natl Acad Sci U S A 108 : 7183 7188.
60. Hirakawa H,, Harwood CS,, Pechter KB,, Schaefer AL,, Greenberg EP . 2012. Antisense RNA that affects Rhodopseudomonas palustris quorum-sensing signal receptor expression. Proc Natl Acad Sci U S A 109 : 12141 12146.
61. Schaefer AL,, Lappala CR,, Morlen RP,, Pelletier DA,, Lu TY,, Lankford PK,, Harwood CS,, Greenberg EP . 2013. LuxR- and luxI-type quorum-sensing circuits are prevalent in members of the Populus deltoides microbiome. Appl Environ Microbiol 79 : 5745 5752.
62. Schaefer AL,, Oda Y,, Coutinho BG,, Pelletier DA,, Weiburg J,, Venturi V,, Greenberg EP,, Harwood CS . 2016. A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides. mBio 7 : e01101-16.
63. Alvarez-Ortega C,, Harwood CS . 2007. Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol Microbiol 65 : 153 165.
64. Starkey M,, Hickman JH,, Ma L,, Zhang N,, De Long S,, Hinz A,, Palacios S,, Manoil C,, Kirisits MJ,, Starner TD,, Wozniak DJ,, Harwood CS,, Parsek MR . 2009. Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191 : 3492 3503.

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