Antibiotic-producing Micrococcales govern the microbiome that inhabits the fur of two- and three-toed sloths
Diego Rojas-Gätjens
Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Search for more papers by this authorKatherine S. Valverde-Madrigal
Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Search for more papers by this authorKeilor Rojas-Jimenez
Escuela de Biología, Universidad de Costa Rica, 11501-2060 San José, Costa Rica
Search for more papers by this authorReinaldo Pereira
Laboratorio Nacional de Nanotecnología (LANOTEC), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Search for more papers by this authorJudy Avey-Arroyo
The Sloth Sanctuary of Costa Rica, Limon, Costa Rica
Search for more papers by this authorCorresponding Author
Max Chavarría
Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Escuela de Química, Universidad de Costa Rica, 11501-2060 San José, Costa Rica
Centro de Investigaciones en Productos Naturales (CIPRONA), Universidad de Costa Rica, 11501-2060 San José, Costa Rica
For correspondence. E-mail [email protected]. Tel. (+506) 2511 8520; Fax (+506) 2253 5020.
Search for more papers by this authorDiego Rojas-Gätjens
Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Search for more papers by this authorKatherine S. Valverde-Madrigal
Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Search for more papers by this authorKeilor Rojas-Jimenez
Escuela de Biología, Universidad de Costa Rica, 11501-2060 San José, Costa Rica
Search for more papers by this authorReinaldo Pereira
Laboratorio Nacional de Nanotecnología (LANOTEC), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Search for more papers by this authorJudy Avey-Arroyo
The Sloth Sanctuary of Costa Rica, Limon, Costa Rica
Search for more papers by this authorCorresponding Author
Max Chavarría
Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, 1174-1200 San José, Costa Rica
Escuela de Química, Universidad de Costa Rica, 11501-2060 San José, Costa Rica
Centro de Investigaciones en Productos Naturales (CIPRONA), Universidad de Costa Rica, 11501-2060 San José, Costa Rica
For correspondence. E-mail [email protected]. Tel. (+506) 2511 8520; Fax (+506) 2253 5020.
Search for more papers by this authorSummary
Sloths have a dense coat on which insects, algae and fungi coexist in a symbiotic relationship. This complex ecosystem requires different levels of controls; however, most of these mechanisms remain unknown. We investigated the bacterial communities inhabiting the hair of two- (Choloepus Hoffmanni) and three-toed (Bradypus variegatus) sloths and evaluated their potential for producing antibiotic molecules capable of exerting control over the hair microbiota. The analysis of 16S rRNA amplicon sequence variants revealed that the communities in both host species are dominated by Actinobacteriota and Firmicutes. The most abundant genera were Brevibacterium, Kocuria/Rothia, Staphylococcus, Rubrobacter, Nesterenkonia and Janibacter. Furthermore, we isolated nine strains of Brevibacterium and Rothia capable of producing substances that inhibited the growth of common mammalian pathogens. The analysis of the biosynthetic gene clusters of these nine isolates suggests that the pathogen-inhibitory activity could be mediated by the presence of siderophores, terpenes, beta-lactones, Type III polyketide synthases, ribosomally synthesized and post-translationally modified peptides, non-alpha poly-amino acids like e-Polylysine, ectoine or non-ribosomal peptides. Our data suggest that Micrococcales that inhabit sloth hair could have a role in controlling microbial populations in that habitat, improving our understanding of this highly complex ecosystem.
Supporting Information
Filename | Description |
---|---|
emi16082-sup-0001-AppendixS1.docxWord 2007 document , 23.2 KB | Appendix S1. Supporting Information. |
emi16082-sup-0002-FigureS1.tifimage/tif, 26.7 KB | Fig. S1. Diversity measures of the hair samples from Bradypus variegatus and Choloepus hoffmanni. The diversity measures (Shannon, Simpson and Observed Richness) were calculated using phyloseq. Figure shows A) diversity measures of all samples grouped by sample point. B) Diversity measures of all samples. |
emi16082-sup-0003-FigureS2.tifimage/tif, 876.3 KB | Fig. S2. Taxonomic composition at the family level of prokaryotic community inhabiting the hair of Bradypus variegatus and Choloepus hoffmanni. Relative abundance of bacterial and archaeal organisms at the family level. The ASV were taxonomically classified using SILVA reference database v138 (Quast et al., 2013) as described in ‘Experimental procedures’. Bradypus samples are identified as B1 to B13 and Choloepus samples are identified as C1-C15. |
emi16082-sup-0004-FigureS3.tifimage/tif, 5.7 MB | Fig. S3. Isolates that present antimicrobial activity found in the hair of Bradypus variegatus and Choloepus hoffmanni. Bacteria were grown on ISP2 agar for 1 week. All bacteria are classified either as Brevibacterium, Kocuria or Rothia according to its 16S rRNA sequence. |
emi16082-sup-0005-TableS1.xlsxExcel 2007 spreadsheet , 11.9 KB | Table S1. Metadata of sloths sample on the sloth sanctuary. |
emi16082-sup-0006-TableS2.csvCSV document, 2.3 MB | Table S2. DNA sequence and phylogenetic assignment of the most abundant ASVs detected in the hair samples using Illumina-based amplicon deep-sequencing. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Albuquerque, L., Johnson, M.M., Schumann, P., Rainey, F.A., and da Costa, M.S. (2014) Description of two new thermophilic species of the genus Rubrobacter, Rubrobacter calidifluminis sp. nov. and Rubrobacter naiadicus sp. nov., and emended description of the genus Rubrobacter and the species Rubrobacter bracarensis. Syst Appl Microbiol 37: 235–243.
- Amiri, H., Azarbaijani, R., Parsa Yeganeh, L., Shahzadeh Fazeli, A., Tabatabaei, M., Salekdeh, G.H., and Karimi, K. (2016) Nesterenkonia sp. strain F, a halophilic bacterium producing acetone, butanol, and ethanol under aerobic conditions. Sci Rep 6: e18408.
- Apostolopoulos, N., Glaeser, S.P., Bagwe, R., Janssen, S., Mayer, U., Ewers, C., et al. (2021) Description and comparison of the skin and ear canal microbiota of non-allergic and allergic German shepherd dogs using next generation sequencing. PLoS One 16: e0250695.
- Arfi, K., Amárita, F., Spinnler, H.E., and Bonnarme, P. (2003) Catabolism of volatile sulfur compounds precursors by Brevibacterium linens and Geotrichum candidum, two microorganisms of the cheese ecosystem. J Biotechnol 105: 245–253.
- Asai, N., Suematsu, H., Yamada, A., Watanabe, H., Nishiyama, N., Sakanashi, D., et al. (2019) Brevibacterium paucivorans bacteremia: case report and review of the literature. BMC Infect Dis 19: e344.
- Bal, Z.S., Sen, S., Karapinar, D.Y., Aydemir, S., and Vardar, F. (2015) The first reported catheter-related Brevibacterium casei bloodstream infection in a child with acute leukemia and review of the literature. Braz J Infect Dis 19: 213–215.
- Belheouane, M., Vallier, M., Čepić, Chung, C.J., Ibrahim, S., and Baines, J.F. (2020) Assessing similarities and disparities in the skin microbiota between wild and laboratory populations of house mice. ISME J 14: 2367–2380.
- Bernal, C., Cairó, J., and Coello, N. (2006) Purification and characterization of a novel exocellular keratinase from Kocuria rosea. Enzyme Microb Technol 38: 49–54.
- Blin, K., Shaw, S., Steinke, K., Villebro, R., Ziemert, N., Lee, S.Y., et al. (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47: 81–87.
- Bradley, C.W., Morris, D.O., Rankin, S.C., Cain, C.L., Misic, A.M., Houser, T., et al. (2016) Longitudinal evaluation of the skin microbiome and association with microenvironment and treatment in canine atopic dermatitis. J Invest Dermatol 136: 1182–1190.
- Brinkac, L., Clarke, T.H., Singh, H., Greco, C., Gomez, A., Torralba, M.G., et al. (2018) Spatial and environmental variation of the human hair microbiota. Sci Rep 8: e9017.
- Buchfink, B., Xie, C., and Huson, D.H. (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12: 59–60.
- Buffoli, B., Rinaldi, F., Labanca, M., Sorbellini, E., Trink, A., Guanziroli, E., et al. (2014) The human hair: from anatomy to physiology. Int J Dermatol 53: 331–341.
- Byrd, A.L., Belkaid, Y., and Segre, J.A. (2018) The human skin microbiome. Nat Rev Microbiol 16: 143–155.
- Cambronero-Heinrichs, J.C., Matarrita-Carranza, B., Murillo-Cruz, C., Araya-Valverde, E., Chavarría, M., and Pinto-Tomás, A.A. (2019) Phylogenetic analyses of antibiotic-producing Streptomyces sp. isolates obtained from the stingless-bee Tetragonisca angustula (Apidae: Meliponini). Microbiology 165: 292–301.
- Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., et al. (2010) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108: 4516–4522.
- Carreto, L., Moore, E., Nobre, M.F., Wait, R., Riley, P.W., Sharp, R.J., and Da Costa, M.S. (1996) Rubrobacter xylanophilus sp. nov., a new thermophilic species isolated from a thermally polluted effluent. Int J Syst Evol Microbiol 46: 460–465.
- Carson, D.A., Barkema, H.W., Naushad, S., and De Buck, J. (2017) Bacteriocins of non-aureus Staphylococci isolated from bovine milk. Appl Environ Microbiol 8: e01015-17.
- Chander, A.M., Nair, R.G., Kaur, G., Kochhar, R., Dhawan, D.K., Bhadada, S.K., and Mayilraj, S. (2017) Genome insight and comparative pathogenomic analysis of Nesterenkonia jeotgali strain CD08_7 isolated from duodenal mucosa of celiac disease patient. Front Microbiol 8: 129.
- Chen, M.Y., Wu, S.H., Lin, G.H., Lu, C.P., Lin, Y.T., Chang, W.C., and Tsay, S.S. (2004) Rubrobacter taiwanensis sp. nov., a novel thermophilic, radiation-resistant species isolated from hot springs. Int J Syst Evol Microbiol 54: 1849–1855.
- Chen, P., Zhang, L., Wang, J., Ruan, J., Han, X., and Huang, Y. (2016) Brevibacterium sediminis sp. nov., isolated from deep-sea sediments from the Carlsberg and Southwest Indian Ridges. Int J Syst Evol Microbiol 66: 5268–5274.
- Chen, Y.E., Fischbach, M.A., and Belkaid, Y. (2018) Skin microbiota-host interactions. Nature 553: 427–436.
- Chermprapai, S., Ederveen, T., Broere, F., Broens, E.M., Schlotter, Y.M., van Schalkwijk, S., et al. (2019) The bacterial and fungal microbiome of the skin of healthy dogs and dogs with atopic dermatitis and the impact of topical antimicrobial therapy, an exploratory study. Vet Microbiol 229: 90–99.
- Chun, J., and Goodfellow, M. (1995) A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Evol Microbiol 45: 240–245.
- Cogen, A.L., Nizet, V., and Gallo, R.L. (2008) Skin microbiota: a source of disease or defense? Brit J Dermatol 158: 442–455.
- Collins, M.D., Farrow, J.A., Goodfellow, M., and Minnikin, D.E. (1983) Brevibacterium casei sp. nov. and Brevibacterium epidermidis sp. nov. Syst Appl Microbiol 4: 388–395.
- Collins, M.D., Hutson, R.A., Båverud, V., and Falsen, E. (2000) Characterization of a Rothia-like organism from a mouse: description of Rothia nasimurium sp. nov. and reclassification of Stomatococcus mucilaginosus as Rothia mucilaginosa comb. nov. Int J Syst Evol Microbiol 50: 1247–1251.
- Council, S.E., Savage, A.M., Urban, J.M., Ehlers, M.E., Skene, J.H., Platt, M.L., et al. (2016) Diversity and evolution of the primate skin microbiome. Proc Biol Sci 283: 20152586.
- Dastager, S.G., Krishnamurthi, S., Rameshkumar, N., and Dharne, M. (2014) The family Micrococcaceae. In The Prokaryotes, E. Rosenberg, E.F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (eds). Berlin, Heidelberg: Springer.
- Dawson, T.J., Webster, K.N., and Maloney, S.K. (2014) The fur of mammals in exposed environments; do crypsis and thermal needs necessarily conflict? The polar bear and marsupial koala compared. J Comp Physiol B 184: 273–284.
- De Oliveira Moreira, D., Leite, G.R., de Siqueira, M.F., Coutinho, B.R., Zanon, M.S., and Mendes, S.L. (2014) The distributional ecology of the maned sloth: environmental influences on its distribution and gaps in knowledge. PLoS One 9: e110929.
- Dill-McFarland, K.A., Weimer, P.J., Pauli, J.N., Peery, M.Z., and Suen, G. (2016) Diet specialization selects for an unusual and simplified gut microbiota in two-and three-toed sloths. Environ Microbiol 18: 1391–1402.
- Downie, M.M., and Kealey, T. (2004) Human sebaceous glands engage in aerobic glycolysis and glutaminolysis. Brit J Dermatol 151: 320–327.
- Duan, Y., Wu, F., Wang, W., He, D., Gu, J.D., Feng, H., et al. (2017) The microbial community characteristics of ancient painted sculptures in Maijishan Grottoes, China. PLoS One 12: e0183598.
- Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
- Edouard, S., Sankar, S., Dangui, N.P., Lagier, J.C., Michelle, C., Raoult, D., and Fournier, P.E. (2014) Genome sequence and description of Nesterenkonia massiliensis sp. nov. strain NP1(T.). Stand Genomic Sci 9: 866–882.
- Falconi, N., Vieira, E.M., Baumgarten, J., Faria, D., and Fernandez Giné, G.A. (2015) The home range and multi-scale habitat selection of the threatened maned three-toed sloth (Bradypus torquatus). Mamm Biol 80: 431–439.
- Ferreira, A.C., Nobre, M.F., Moore, E., Rainey, F.A., Battista, J.R., and da Costa, M.S. (1999) Characterization and radiation resistance of new isolates of Rubrobacter radiotolerans and Rubrobacter xylanophilus. Extremophiles 3: 235–238.
- Forquin, M.P., Duvergey, H., Proux, C., Loux, V., Mounier, J., Landaud, S., et al. (2009) Identification of brevibacteriaceae by multilocus sequence typing and comparative genomic hybridization analyses. Appl Environ Microbiol 75: 6406–6409.
- Forquin-Gomez, M.P., Weimer, B.C., Sorieul, L., Kalinowski, J., and Vallaeys, T. (2014) The family Brevibacteriaceae. In The Prokaryotes, E. Rosenberg, E.F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (eds). Heidelberg: Springer, Berlin.
- Gaiser, R.A., Medema, M.H., Kleerebezem, M., van Baarlen, P., and Wells, J.M. (2017) Draft genome sequence of a porcine commensal, Rothia nasimurium, encoding a nonribosomal peptide synthetase predicted to produce the ionophore antibiotic valinomycin. Genome Announc 5: e00453-17.
- Gellatly, S.L., and Hancock, R.E. (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67: 159–173.
- Gohli, J., Bøifot, K.O., Moen, L.V., Pastuszek, P., Skogan, G., Udekwu, K.I., and Dybwad, M. (2019) The subway microbiome: seasonal dynamics and direct comparison of air and surface bacterial communities. Microbiome 7: e160.
- Grice, E.A., and Segre, J.A. (2011) The skin microbiome. Nat Rev Microbiol 9: 244–253.
- Hansen, B.G. (1985) Etiologic importance of coagulase-negative Micrococcaceae isolated from blood cultures. Acta Pathol Microbiol Immunol Scand B 93: 1–6.
- Hassoun, A., Linden, P.K., and Friedman, B. (2017) Incidence, prevalence, and management of MRSA bacteremia across patient populations-a review of recent developments in MRSA management and treatment. Critical Care 21: e211.
- Heyrman, J., Verbeeren, J., Schumann, P., Devos, J., Swings, J., and De Vos, P. (2004) Brevibacterium picturae sp. nov., isolated from a damaged mural painting at the Saint-Catherine chapel (Castle Herberstein, Austria). Int J Syst and Evol Microbiol 54: 1537–1541.
- Higginbotham, S., Wong, W.R., Linington, R.G., Spadafora, C., Iturrado, L., Spadafora, C., et al. (2014) Sloth hair as a novel source of fungi with potent anti-parasitic, anti-cancer and anti-bacterial bioactivity. PLoS One 9: e84549.
- Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: e119.
- Ianiri, G., Coelho, M.A., Ruchti, F., Sparber, F., McMahon, T.J., Fu, C., et al. (2020) HGT in the human and skin commensal Malassezia: a bacterially derived flavohemoglobin is required for NO resistance and host interaction. Proc Natl Acad Sci U S A 117: 15884–15894.
- Jensen, P.R., Gontang, E., Mafnas, C., Mincer, T.J., and Fenical, W. (2005) Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environ Microbiol 7: 1039–1048.
- Johnson, L.S., Eddy, S.R., and Portugaly, E. (2010) Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11: e431.
- Jurado, V., Miller, A.Z., Alias-Villegas, C., Laiz, L., and Saiz-Jimenez, C. (2012) Rubrobacter bracarensis sp. nov., a novel member of the genus Rubrobacter isolated from a biodeteriorated monument. Syst Appl Microbiol 35: 306–309.
- Kämpfer, P., Glaeser, S.P., Busse, H.J., Abdelmohsen, U.R., and Hentschel, U. (2014) Rubrobacter aplysinae sp. nov., isolated from the marine sponge Aplysina aerophoba. Int J Syst Evol Microbiol 64: 705–709.
- Kandi, V., Palange, P., Vaish, R., Bhatti, A.B., Kale, V., Kandi, M.R., and Bhoomagiri, M.R. (2016) Emerging bacterial infection: identification and clinical significance of Kocuria species. Cureus 8: e731.
- Katı, H., İnce, İ.A., Demir, İ., and Demirbağ, Z. (2010) Brevibacterium pityocampae sp. nov., isolated from caterpillars of Thaumetopoea pityocampa (Lepidoptera, Thaumetopoeidae). Int J Syst Evol Microbiol 60: 312–316.
- Kaur, C., Kaur, I., Raichand, R., Bora, T.C., and Mayilraj, S. (2011) Description of a novel actinobacterium Kocuria assamensis sp. nov., isolated from a water sample collected from the river Brahmaputra, Assam, India. Antonie van Leeuwenhoek 99: 721–726.
- Kim, S.B., Nedashkovskaya, O.I., Mikhailov, V.V., Han, S.K., Kim, K.O., Rhee, M.S., and Bae, K.S. (2004) Kocuria marina sp. nov., a novel actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 54: 1617–1620.
- Kloos, W.E., Zimmerman, R.J., and Smith, R.F. (1976) Preliminary studies on the characterization and distribution of Staphylococcus and Micrococcus species on animal skin. Appl Environ Microbiol 31: 53–59.
- Lahti L., and Shetty S. (2018) Introduction to the microbiome R package. URL http://bioconductor.statistik.tu-dortmund.de/packages/3.6/bioc/vignettes/microbiome/inst/doc/vignette.html.
- Li, D., Luo, R., Liu, C.M., Leung, C.M., Ting, H.F., Sadakane, K., et al. (2016) MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102: 3–11.
- Liu, Q., Liu, Q., Meng, H., Lv, H., Liu, Y., Liu, J., et al. (2020) Staphylococcus epidermidis contributes to healthy maturation of the nasal microbiome by stimulating antimicrobial peptide production. Cell Host Microbe 27: 68–78.
- Lory, S. (2014) The family Staphylococcaceae. In The Prokaryotes, E. Rosenberg, E.F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (eds). Berlin, Heidelberg: Springer.
- Lousada, M.B., Lachnit, T., Edelkamp, J., Rouillé, T., Ajdic, D., Uchida, Y., et al. (2021) Exploring the human hair follicle microbiome. Brit J Dermatol 184: 802–815.
- Ma, X., Li, G., Yang, C., He, M., Wang, C., Gu, Y., et al. (2021) Skin microbiota of the captive giant panda (Ailuropoda Melanoleuca) and the distribution of opportunistic skin disease-associated bacteria in different seasons. Front Vet Sci 8: 666486. https://doi.org/10.3389/fvets.2021.666486.
- Maisnier-Patin, S., and Richard, J. (1995) Activity and purification of linenscin OC2, an antibacterial substance produced by Brevibacterium linens OC2, an orange cheese coryneform bacterium. Appl Environ Microbiol 61: 1847–1852.
- Matarrita-Carranza, B., Murillo-Cruz, C., Avendaño, R., Ríos, M.I., Chavarría, M., Gómez-Calvo, M.L., et al. (2021) Streptomyces sp. M54: an actinobacteria associated with a neotropical social wasp with high potential for antibiotic production. Antonie Van Leeuwenhoek 114: 379–398.
- Mendoza, J.E., Peery, M.Z., Gutiérrez, G.A., Herrera, G., and Pauli, J.N. (2015) Resource use by the two-toed sloth (Choloepus hoffmanni) and the three-toed sloth (Bradypus variegatus) differs in a shade-grown agro-ecosystem. J Trop Ecol 31: 49–55.
- Molina-Mora, J.A., Chinchilla-Montero, D., Chavarría-Azofeifa, M., Ulloa-Morales, A.J., Campos-Sánchez, R., Mora-Rodríguez, R., et al. (2020) Transcriptomic determinants of the response of ST-111 Pseudomonas aeruginosa AG1 to ciprofloxacin identified by a top-down systems biology approach. Sci Rep 10: e13717.
- Mounier, J., Rea, M.C., O'Connor, P.M., Fitzgerald, G.F., and Cogan, T.M. (2007) Growth characteristics of Brevibacterium, Corynebacterium, Microbacterium, and Staphylococcus spp. isolated from surface-ripened cheese. Appl Environ Microbiol 73: 7732–7739.
- Newstead, L.L., Varjonen, K., Nuttall, T., and Paterson, G.K. (2020) Staphylococcal-produced bacteriocins and antimicrobial peptides: their potential as alternative treatments for Staphylococcus aureus infections. Antibiotics 9: e40.
- Nguyen, T.H., Park, M.D., and Otto, M. (2017) Host response to Staphylococcus epidermidis colonization and infections. Front Cell Infect Microbiol 7: e90.
- Nouioui, I., Carro, L., García-López, M., Meier-Kolthoff, J.P., Woyke, T., Kyrpides, N.C., et al. (2018) Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 9: e2007.
- Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P. M., Stevens, M.H.H., Szoecs, E., and Wagner, H. (2019) Vegan: community ecology package. R package version 2:5–6. URL https://cran.r-project.org/web/packages/vegan/index.html.
- O'Sullivan, J.N., Rea, M.C., O'Connor, P.M., Hill, C., and Ross, R.P. (2019) Human skin microbiota is a rich source of bacteriocin-producing staphylococci that kill human pathogens. FEMS Microbiol Ecol 95: fiy241.
- Pauli, J.N., Mendoza, J.E., Steffan, S.A., Carey, C.C., Weimer, P.J., and Peery, M.Z. (2014) A syndrome of mutualism reinforces the lifestyle of a sloth. Proc R Soc B 281: e20133006.
- Polak-Witka, K., Rudnicka, L., Blume-Peytavi, U., and Vogt, A. (2020) The role of the microbiome in scalp hair follicle biology and disease. Exp Dermatol 29: 286–294.
- Price, M.N., Dehal, P.S., and Arkin, A.P. (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641–1650.
- Pridham, T.G., Anderson, P., Foley, C., Lindenfelser, L.A., Hesseltine, C.W., and Benedict, R.G. (1957) A selection of media for maintenance and taxonomic study of streptomycetes. Antibiot Annu 1957: 947–953.
- Qiu, X., Kulasekara, B.R., and Lory, S. (2009) Role of horizontal gene transfer in the evolution of Pseudomonas aeruginosa virulence. Genome Dyn 6: 126–139.
- Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: 590–596.
- R Core Team. (2019) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.r-project.org/.
- Ramanan, P., Barreto, J.N., Osmon, D.R., and Tosh, P.K. (2014) Rothia bacteremia: a 10-year experience at Mayo Clinic, Rochester, Minnesota. J Clin Microbiol 52: 3184–3189.
- Reddy, G., Prakash, J., Prabahar, V., Matsumoto, G.I., Stackebrandt, E., and Shivaji, S. (2003) Kocuria polaris sp. nov., an orange-pigmented psychrophilic bacterium isolated from an Antarctic cyanobacterial mat sample. Int J Syst Evol Microbiol 53: 183–187.
- Rodrigues, H.A. (2017) The cutaneous ecosystem: the roles of the skin microbiome in health and its association with inflammatory skin conditions in humans and animals. Vet Dermatol 28: 60–e15.
- Rojas-Gätjens, D., Fuentes-Schweizer, P., Rojas-Jiménez, K., Pérez-Pantoja, D., Avendaño, R., Alpízar, R., et al. (2022) Methylotrophs and hydrocarbon-degrading bacteria are key players in the microbial community of an abandoned century-old oil exploration well. Microb Ecol 83: 83–99.
- Ross, A.A., Müller, K.M., Weese, J.S., and Neufeld, J.D. (2018) Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class Mammalia. Proc Natl Acad Sci U S A 115: 5786–5795.
- Ross, A.A., Rodrigues Hoffmann, A., and Neufeld, J.D. (2019) The skin microbiome of vertebrates. Microbiome 7: e79.
- Roux, V., and Raoult, D. (2009) Brevibacterium massiliense sp. nov., isolated from a human ankle discharge. Int J Syst Evol Microbiol 59: 1960–1964.
- Sanford, J.A., and Gallo, R.L. (2013) Functions of the skin microbiota in health and disease. Semin Immunol 25: 370–377.
- Saxena, R., Mittal, P., Clavaud, C., Dhakan, D.B., Roy, N., Breton, L., et al. (2021) Longitudinal study of the scalp microbiome suggests coconut oil to enrich healthy scalp commensals. Sci Rep 11: e7220.
- Singh, H., Du, J., Yang, J.E., Shik Yin, C., Kook, M., and Yi, T.H. (2016) Brachybacterium horti sp. nov., isolated from garden soil. Int J Syst Evol Microbiol 66: e189–e195.
- Stackebrandt, E. (2014) The family Dermabacteraceae. In The Prokaryotes, E. Rosenberg, E.F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (eds). Berlin, Heidelberg: Springer.
- Stackebrandt, E., Koch, C., Gvozdiak, O., and Schumann, P. (1995) Taxonomic dissection of the genus Micrococcus: Kocuria gen. nov., Nesterenkonia gen. nov., Kytococcus gen. nov., Dermacoccus gen. nov., and Micrococcus Cohn 1872 gen. emend. Int J Syst Bacteriol 45: 682–692.
- Sun, Y., Shi, Y.L., Wang, H., Zhang, T., Yu, L.Y., Sun, H., and Zhang, Y.Q. (2018) Diversity of bacteria and the characteristics of Actinobacteria community structure in Badain Jaran desert and Tengger desert of China. Front Microbiol 9: e1068.
- Suutari, M., Majaneva, M., Fewer, D.P., Voirin, B., Aiello, A., Friedl, T., et al. (2010) Molecular evidence for a diverse green algal community growing in the hair of sloths and a specific association with Trichophilus welckeri (Chlorophyta, Ulvophyceae). BMC Evol Biol 10: e86.
- Tak, E.J., Kim, P.S., Hyun, D.W., Kim, H.S., Lee, J.Y., Kang, W., et al. (2018) Phenotypic and genomic properties of Brachybacterium vulturis sp. nov. and Brachybacterium avium sp. nov. Front Microbiol 9: e1809.
- Talento, A.F., Malnick, H., Cotter, M., Brady, A., McGowan, D., Smyth, E., and Fitzpatrick, F. (2013) Brevibacterium otitidis: an elusive cause of neurosurgical infection. J Med Microbiol 62: 486–488.
- Taube, E., Keravec, J., Vié, J.C., and Duplantier, J.M. (2008) Reproductive biology and postnatal development in sloths, Bradypus and Choloepus: review with original data from the field (French Guiana) and from captivity. Mamm Rev 31: 173–188.
10.1111/j.1365-2907.2001.00085.x Google Scholar
- Thi, M., Wibowo, D., and Rehm, B. (2020) Pseudomonas aeruginosa Biofilms. Int J Mol Sci 21: e8671.
- Uranga, C.C., Arroyo, P., Jr., Duggan, B.M., Gerwick, W.H., and Edlund, A. (2020) Commensal oral Rothia mucilaginosa produces enterobactin, a metal-chelating siderophore. mSystems 5: e00161-20.
- Valdés-Stauber, N., and Scherer, S. (1994) Isolation and characterization of Linocin M18, a bacteriocin produced by Brevibacterium linens. Appl Environ Microbiol 60: 3809–3814.
- Vaughan, C., Ramírez, O., Herrera, G., and Guries, R. (2007) Spatial ecology and conservation of two sloth species in a cacao landscape in limón, Costa Rica. Biodivers Conserv 16: 2293–2310.
- Waage, J.F., and Montgomery, G. (1976) Cryptoses choloepi: a coprophagous moth that lives on a Sloth. Science 193: 157–158.
- Watanabe, K., Yamada, A., Nishi, Y., Tashiro, Y., and Sakai, K. (2021) Host factors that shape the bacterial community structure on scalp hair shaft. Sci Rep 11: e17711.
- Wujek, D.E., and Cocuzza, J.M. (1986) Morphology of hair of two- and three-toe sloths (Edentata: Bradypodidae). Rev Biol Trop 34: 243–246.