Sulphate-reducing　microorganisms,　or　SRMs,　are　crucial　to　organic　decomposition,　the　sulphur　cycle,　and　the　formation　of　pyrite.　Despite　their　low　energy-yielding　metabolism　and　intense　competition　with　other　microorganisms,　their　ability　to　thrive　in　natural　habitats　often　lacking　sufficient　substrates　remains　an　enigma.　This　study　delves　into　how　Desulfovibrio　desulfuricans　G20,　a　representative　SRM,　utilizes　photoelectrons　from　extracellular　sphalerite　(ZnS),　a　semiconducting　mineral　that　often　coexists　with　SRMs,　for　its　metabolism　and　energy　production.　Batch　experiments　with　sphalerite　reveal　that　the　initial　rate　and　extent　of　sulphate　reduction　by　G20　increased　by　3.6　and　3.2　times　respectively　under　light　conditions　compared　to　darkness,　when　lactate　was　not　added.　Analyses　of　microbial　photoelectrochemical,　transcriptomic,　and　metabolomic　data　suggest　that　in　the　absence　of　lactate,　G20　extracts　photoelectrons　from　extracellular　sphalerite　through　cytochromes,　nanowires,　and　electron　shuttles.　Genes　encoding　movement　and　biofilm　formation　are　upregulated,　suggesting　that　G20　might　sense　redox　potential　gradients　and　migrate　towards　sphalerite　to　acquire　photoelectrons.　This　process　enhances　the　intracellular　electron　transfer　activity,　sulphur　metabolism,　and　ATP　production　of　G20,　which　becomes　dominant　under　conditions　of　carbon　starvation　and　extends　cell　viability　in　such　environments.　This　mechanism　could　be　a　vital　strategy　for　SRMs　to　survive　in　energy-limited　environments　and　contribute　to　sulphur　cycling.　©　2024　John　Wiley　&　Sons　Ltd.