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Sookie Stackhouse (Anna Paquin) is a waitress with telepathic abilities. Stephen Moyer plays her love interest, vampire Bill Compton. Sookie works for Sam Merlotte, played by Sam Trammell, owner of Merlotte's bar and a shapeshifter who has a crush on Sookie. Rutina Wesley plays Sookie's best friend Tara Thornton, begins bartending at Merlotte's after quitting her job at the Super Save-A-Bunch. Also working at Merlotte's are Tara's cousin Lafayette Reynolds, played by Nelsan Ellis, a short order cook and hustler, and Arlene Fowler, played by Carrie Preston. Arlene is a thrice-divorced waitress with two children who, over the course of the season, becomes engaged to Rene Lenier, played by Michael Raymond-James, a Cajun labourer who works on a road crew.
Ryan Kwanten plays Jason Stackhouse, Sookie's brother, a labourer on a road crew and ladies' man. Jason's sexual conquests begin to die, one after the other, and he is suspected of being a serial killer. Jim Parrack is Hoyt Fortenberry, Jason's co-worker who admires Jason's abilities with women. Lois Smith plays Adele Stackhouse, Jason and Sookie's grandmother who has looked after them since the deaths of their parents. Lizzy Caplan plays Jason's love interest Amy Burley, who begins a relationship with Jason because of a shared addiction to vampire blood, or "V". They kidnap Eddie Gauthier, played by Stephen Root, to use his blood.
In the vampire community Alexander Skarsgård plays Eric Northman, the Sheriff of Area 5, which includes Bon Temps, and owner of the vampire bar Fangtasia. Working for Eric, both in the bar and under him as Sheriff, are Pam, played by Kristin Bauer, and Chow, played by Patrick Gallagher. The bartender Longshadow, played by Raoul Trujillo, is killed by Bill to protect Sookie. As punishment for killing a fellow vampire and to replenish the vampire ranks, Bill is taken to the Magister, played by Željko Ivanek, and forced to sire Jessica Hamby, played by Deborah Ann Woll. Jessica is cared for by Eric but when he grows tired of her he leaves her with Bill.
In the middle of the season Tara's mother, Lettie Mae, played by Adina Porter, undergoes an exorcism to rid herself of what she terms her "demons" - her addiction to alcohol. The exorcism is administered by "Miss Jeanette" an alias of Nancy LeGuare, played by Aisha Hinds. Following her exorcism Lettie Mae kicks Tara out. Following a crash and DUI, Tara is taken in by Maryann Forrester (who initially presents herself to Tara as some kind of social worker), played by Michelle Forbes. While staying with Maryann, Tara meets "Eggs" Benedict Talley, played by Mehcad Brooks, to whom she feels a strong attraction.
The central mystery of the season begins when Maudette Pickens, played by Danielle Sapia, is killed. William Sanderson plays Sheriff Dearborne, who places his only detective, Andy Bellefleur, played by Chris Bauer, in charge of finding the killer. Bellefleur suspects Jason Stackhouse, and that suspicion grows after the murder of Dawn Green, played by Lynn Collins. Andy's cousin Terry, played by Todd Lowe, works as a cook at Merlotte's.
Other minor characters include Mack and Denise Rattray, played by James Jean Parks and Karina Logue. Bartlett Hale played by Cheyenne Wilbur, Sookie and Jason's pedophile great-uncle. Coroner's assistant Neil Jones played by Kevin Michael McHale, and vampires Malcolm, Liam and Diane played by Andrew Rothenberg, Graham Shiels and Aunjanue Ellis.
The international conflict between vampires and humans is played out in the background, but two minor characters are introduced who become major characters in the second season. Michael McMillian plays Reverend Steve Newlin and Anna Camp plays his wife Sarah. They head the anti-vampire church the Fellowship of the Sun following the death of Steve's father, who was supposedly killed by vampires. A representative of the Fellowship of the Sun approaches Jason Stackhouse while he is in jail in the final episode of the season.