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MBio. 2018 Oct 9;9(5). pii: e01432-18. doi: 10.1128/mBio.01432-18.

A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes.

Wood DLA#1, Lachner N#1, Tan JM2,3,4,5, Tang S2,3,4,5, Angel N1, Laino A2,3,4,5, Linedale R4,5, Lê Cao KA4,5,6, Morrison M4,5, Frazer IH2,3,4,5, Soyer HP2,3,4,5, Hugenholtz P7,4,5.

Author information

1
Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia.
2
Dermatology Research Centre, The University of Queensland, Brisbane, Queensland, Australia.
3
Dermatology Department, Princess Alexandra Hospital, Brisbane, Queensland, Australia.
4
Diamantina Institute, The University of Queensland, Brisbane, Queensland, Australia.
5
Translational Research Institute, The University of Queensland, Brisbane, Queensland, Australia.
6
School of Mathematics and Statistics, Melbourne Integrative Genomics, The University of Melbourne, Victoria, Australia.
7
Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia p.hugenholtz@uq.edu.au.
#
Contributed equally

Abstract

Cutaneous squamous cell carcinoma (SCC) is the second-most-common cancer in Australia. The majority of SCCs progress from premalignant actinic keratosis (AK) lesions that form on chronically sun-exposed skin. The role of skin microbiota in this progression is not well understood; therefore, we performed a longitudinal microbiome analysis of AKs and SCCs using a cohort of 13 SCC-prone immunocompetent men. The majority of variability in microbial profiles was attributable to subject, followed by time and lesion type. Propionibacterium and Malassezia organisms were relatively more abundant in nonlesional photodamaged skin than in AKs and SCCs. Staphylococcus was most commonly associated with lesional skin, in particular, sequences most closely related to Staphylococcus aureus Of 11 S. aureus-like operational taxonomic units (OTUs), six were significantly associated with SCC lesions across seven subjects, suggesting their specific involvement with AK-to-SCC progression. If a causative link exists between certain S. aureus-like OTUs and SCC etiology, therapeutic approaches specifically targeting these bacteria could be used to reduce SCC.IMPORTANCE Actinic keratosis (AK) and cutaneous squamous cell carcinoma (SCC) are two of the most common dermatologic conditions in Western countries and cause substantial morbidity worldwide. The role of human papillomaviruses under these conditions has been well studied yet remains inconclusive. One PCR-based study has investigated bacteria in the etiology of these conditions; however, no study has investigated the microbiomes of AK and SCC more broadly. We longitudinally profiled the microbiomes of 112 AK lesions, profiled cross sections of 32 spontaneously arising SCC lesions, and compared these to matching nonlesional photodamaged control skin sites. We identified commonly occurring strains of Propionibacterium and Malassezia at higher relative abundances on nonlesional skin than in AK and SCC lesions, and strains of Staphylococcus aureus were relatively more abundant in lesional than nonlesional skin. These findings may aid in the prevention of SCC.

KEYWORDS:

16S RNA; Malassezia ; Staphylococcus aureus ; actinic keratosis; microbiome; skin; squamous cell carcinoma

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