Opsins are photosensitive proteins catalyzing light-dependent processes across the tree of life. For both microbial (type 1) and metazoan (type 2) opsins, photosensing depends upon covalent interaction between a retinal chromophore and a conserved lysine residue. Despite recent discoveries of potential opsin homologs lacking this residue, phylogenetic dispersal and functional significance of these abnormal sequences have not yet been investigated. We report discovery of a large group of putatively non-retinal binding opsins, present in a number of fungal and microbial genomes and comprising nearly 30% of opsins in the Halobacteriacea, a model clade for opsin photobiology. We report phylogenetic analyses, structural modeling, genomic context analysis and biochemistry, to describe the evolutionary relationship of these recently described proteins with other opsins, show that they are expressed and do not bind retinal in a canonical manner. Given these data, we propose a hypothesis that these abnormal opsin homologs may represent a novel family of sensory opsins which may be involved in taxis response to one or more non-light stimuli. If true, this finding would challenge our current understanding of microbial opsins as a light-specific sensory family, and provides a potential analogy with the highly diverse signaling capabilities of the eukaryotic G-protein coupled receptors (GPCRs), of which metazoan type 2 opsins are a light-specific sub-clade. SI_Dataset_1_Haloarcheal_opsin_seqsFasta file containing 170 haloarchaeal opsin sequences recovered by BLASTp searches of haloarchaeal genomes, after correcting for incorrectly called start sites. Sequences are marked with tags noting differences from corresponding NCBI records. Long = sequence is longer than corresponding NCBI record. ID_to = sequence perfectly matches multiple NCBI records, Not_ID = sequence is not identical to corresponding NCBI record, Cap = sequence has alternative annotation as “capsular polysaccharide biosynthesis protein”.SI_Dataset_2_Haloarchaeal_opsins_treeNexus formatted phylogeny file for 170 haloarchaeal opsins included in this study. Best opened with FigTree v1.4.0. Corresponds to Fig 2A and SI Fig. 5.SI_Dataset_3_Alignment_halo_trimmedFasta formatted alignment file for 170 haloarchaeal opsins included in this study after manual trimming. Remaining 204 positions were used for phylogenetic inference with MrBayes.SI_Dataset_4_Opsin_related_genes_queriesFasta formatted file containing query sequences used in BLASTp searches for brp, crtE, crtB, crtI, and crtY.SI_Dataset_5_Universal_opsins_treeNexus formatted phylogeny file for 1077 Class I opsins collected from the NCBI nr and env_nr databases. Best opened with FigTree v1.4.0. Corresponds to Fig 2C and SI Fig 3.SI_Dataset_6_Plasmid_sequences.fastaFasta formatted file containing sequences for expression vectors pMTFCHIS2 and pDJLCHIS.