Novel Hawai'i and Pacific Island circulating clusters of Mycobacterium intracellulare subsp. chimaera.

Nontuberculous mycobacteria (NTM) are environmental microorganisms for which large, systematic studies of niche diversity are lacking. We performed a semi-longitudinal state-wide sampling campaign (2015-2019) for environmental NTM across Hawai'i. A volunteer network collected 2,334 water biofilms, soil, and dust samples from built (n = 1,946) and natural (n = 388) sites. Of these, 541 contained culturable NTM (23%) and per island hotspots identified. Of 74 NTM species recovered, the most prevalent rapid growing mycobacteria (RGM) were Mycobacterium porcinum, Mycobacterium chelonae, and Mycobacterium abscessus. Mycobacterium intracellulare subsp. chimaera was the most frequently isolated slow growing mycobacteria (SGM). Our longitudinal analyses indicate widespread colonization of diverse niches by species less associated with lung infections such as M. chelonae. In contrast, household water biofilms tended to be reliable niches for M. abscessus and M. avium complex species colonization across the 5-year study. Analysis of 590 deidentified lung samples from Hawai'i and other Pacific Islands revealed M. chimaera as the most frequently isolated species (40%, 238/590). Phylogenetic analysis of environmental and lung M. abscessus suggests most cluster within dominant circulating clone 1 (DCC1). Contrastingly, most Hawai'i and other Pacific Island M. chimaera were distinct from previously studied European isolates, leading to the identification of two novel clusters of phylogenetically related strains we have termed Pacific Island Circulating Cluster 1 and 2 (PCC1, PCC2). PCC1 consists exclusively of Hawai'i/Pacific Island isolates, while PCC2 was enriched by lung samples and was mostly collected from Hawai'i/Pacific Islands. These data reveal the genetic diversity, ecological niches, and potential reservoirs of NTM in varied Hawai'i ecosystems.IMPORTANCENearly one in four environmental Hawai'i samples tested positive for any NTM species, with hotspots often overlapping population centers. Recovery of any NTM species occurred just as often from natural settings as homes and public buildings, highlighting exposures as a normal part of life. Soil was the most common reservoir for NTM colonization, but we distinguish NTM species pertinent to lung disease that were far more likely to be found in water biofilms, such as showerheads and kitchen sinks. No single species dominated the environment; yet, the type of NTM found in water systems closely mirrored those recovered from patients' lung samples. Genetic analyses revealed that Hawai'i harbors distinct, locally circulating strains, including lineages not linked to known hospital outbreaks. Together, these findings improve our understanding of where precarious exposures can occur and inform public health strategies to reduce exposures by highlighting niches that are common hotspots for NTM colonization.