The PSI-CP43' supercomplex of the cyanobacterium Synechocystis PCC 6803, grown under iron-starvation conditions, consists of a trimeric core Photosystem I (PSI) complex and an outer ring of 18 CP43' light-harvesting complexes. We have investigated the electronic structure and excitation energy transfer (EET) pathways within the CP43' (also known as the isiA gene product) ring using low-temperature absorption, fluorescence, fluorescence excitation, and hole-burning (HB) spectroscopies. Analysis of the absorption spectra of PSI, CP43', and PSI-CP43' complexes suggests that there are 13 chlorophylls (Chls) per CP43' monomer, i.e., a number that was observed in the CP43 complex of Photosystem 11 (PSII) (Umena, Y. et al. Nature 2011, 473, 55-60). This is in contrast with the recent modeling studies of Zhang et al. (Biochim. Biophys. Acta 2010, 1797, 457-465), which suggested that IsiA likely contains 15 Chls. Modeling studies of various optical spectra of the CP43' ring using the uncorrelated EET model (Zazubovich, V.; Jankowiak, R J. Lumin. 2007, 127, 245-250) suggest that CP43' monomers (in analogy to the CP43 complexes of the PSII core) also possess two quasi-degenerate low-energy states, A' and B'. The site distribution functions of states A' and B' maxima/full width at half-maximum (fwhm) are at 684 nm/180 cm(-1) and 683 nm/80 cm(-1), respectively. Our analysis shows that pigments mostly contributing to the lowest-energy A' and B' states must be located on the side of the CP43' complex facing the PSI core, a finding that contradicts the model of Zhang et al. but is in agreement with the model suggested by Nield et al. (Biochemistry 2003, 42, 3180-3188). We demonstrate that the A'-A' and B'-B' EET between different monomers is possible, though with a slower rate than intramonomer A'-B' and/or B'-A' energy transfer.