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Sponges host diverse and complex communities of microbial symbionts that display a high degree of host specificity. The microbiomes of conspecific sponges are relatively constant, even across distant locations, yet few studies have directly examined the influence of abiotic factors on intraspecific variation in sponge microbial community structure. The contrast between intertidal and subtidal environments is an ideal system to assess the effect of environmental variation on sponge-microbe symbioses, producing two drastically different environments on a small spatial scale. Here, we characterized the microbial communities of individual intertidal and subtidal Hymeniacidon heliophila sponges, ambient seawater, and sediment from a North Carolina oyster reef habitat by partial (Illumina sequencing) and nearly full-length (clone libraries) 16S rRNA gene sequence analyses. Clone library sequences were compared to H. heliophila symbiont communities from the Gulf of Mexico and Brazil, revealing strong host specificity of dominant symbiont taxa across expansive geographic distances. Sediment and seawater samples yielded clearly distinct microbial communities from those found in H. heliophila. Despite the close proximity of the sponges sampled, significant differences between subtidal and intertidal sponges in the diversity, structure, and composition of their microbial communities were detected. Differences were driven by changes in the relative abundance of a few dominant microbial symbiont taxa, as well as the presence or absence of numerous rare microbial taxa. These findings suggest that extreme abiotic fluctuations, such as periodic air exposure in intertidal habitats, can drive intraspecific differences in complex host-microbe symbioses., (Copyright © 2016, American Society for Microbiology. All Rights Reserved.)