Abstract
The actinobacterial diversity of Arctic marine sediments was investigated using culture-dependent and culture-independent approaches. A total of 152 strains were isolated from seven different media; 18 isolates were selected for phylogenetic analysis on the basis of their 16S rRNA gene sequences. Results showed that the 18 isolates belonged to a potential novel genus and 10 known genera including Actinotalea, Arthrobacter, Brachybacterium, Brevibacterium, Kocuria, Kytococcus, Microbacterium, Micrococcus, Mycobacterium, and Pseudonocardia. Subsequently, 172 rDNA clones were selected by restriction fragment length polymorphism analysis from 692 positive clones within four actinobacteria-specific 16S rDNA libraries of Arctic marine sediments, and then these 172 clones were sequenced. In total, 67 phylotypes were clustered in 11 known genera of actinobacteria including Agrococcus, Cellulomonas, Demequina, Iamia, Ilumatobacter, Janibacter, Kocuria, Microbacterium, Phycicoccus, Propionibacterium, and Pseudonocardia, along with other, unidentified actinobacterial clones. Based on the detection of a substantial number of uncultured phylotypes showing low BLAST identities (<95 %), this study confirms that Arctic marine environments harbour highly diverse actinobacterial communities, many of which appear to be novel, uncultured species.
Similar content being viewed by others
References
Aiyar A (1999) The use of CLUSTAL W and CLUSTAL X for multiple sequence alignment. In: Misener S, Krawetz SA (eds) Bioinformatics methods and protocols. Methods in molecular biology™, vol vol 132. Humana Press, Totowa, pp 221–241. doi:10.1385/1-59259-192-2:221
Amato P, Hennebelle R, Magand O, Sancelme M, Delort AM, Barbante C, Boutron C, Ferrari C (2007) Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol Ecol 59(2):255–264. doi:10.1111/j.1574-6941.2006.00198.x
Atalan E, Manfio GP, Ward AC, Kroppenstedt RM, Goodfellow M (2000) Biosystematic studies on novel streptomycetes from soil. Antonie Van Leeuwenhoek 77(4):337–353. doi:10.1023/A:1002682728517
Babalola OO, Kirby BM, Le Roes-Hill M, Cook AE, Cary SC, Burton SG, Cowan DA (2009) Phylogenetic analysis of actinobacterial populations associated with Antarctic dry valley mineral soils. Environ Microbiol 11(3):566–576. doi:10.1111/j.1462-2920.2008.01809.x
Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55(3):541–555. doi:10.1016/j.mimet.2003.08.009
Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58(1):1–26. doi:10.1038/ja.2005.1
Brinkmeyer R, Knittel K, Jurgens J, Weyland H, Amann R, Helmke E (2003) Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microbiol 69(11):6610–6619. doi:10.1128/AEM.69.11.6610- 6619.2003
Bull AT, Stach JE, Ward AC, Goodfellow M (2005) Marine actinobacteria: perspectives, challenges, future directions. Antonie Van Leeuwenhoek 87(3):65–79. doi:10.1007/s10482-004-6562-8
Chao A, Shen TJ (2005) Program SPADE (species prediction and diversity estimation). Program and user’s guide. National Tsing Hua University, Taiwan
Fenical W, Jensen PR (2006) Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2(12):666–673. doi:10.1038/nchembio841
Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73(10):3272–3282. doi:10.1128/AEM.02811-06
Goodfellow M, Fiedler HP (2010) A guide to successful bioprospecting: informed by actinobacterial systematics. Antonie Van Leeuwenhoek 98(2):119–142. doi:10.1007/s10482-010-9460-2
Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216. doi:10.1146/annurev.mi.37.100183.001201
Haefner B (2003) Drugs from the deep: marine natural products as drug candidates. Drug Discovery Today 8(12):536–544. doi:10.1016/S1359-6446(03)02713-2
Hames-Kocabas EE, Uzel A (2012) Isolation strategies of marine-derived actinomycetes from sponge and sediment samples. J Microbiol Methods 88(3):342–347. doi:10.1016/j.mimet.2012.01.010
Han SK, Nedashkovskaya OI, Mikhailov VV, Kim SB, Bae KS (2003) Salinibacterium amurskyense gen. nov., sp. nov., a novel genus of the family Microbacteriaceae from the marine environment. Int J Syst Evol Microbiol 53(Pt 6):2061–2066. doi:10.1099/ijs.0.02627-0
Hansen AA, Herbert RA, Mikkelsen K, Jensen LL, Kristoffersen T, Tiedje JM, Lomstein BA, Finster KW (2007) Viability, diversity and composition of the bacterial community in a high Arctic permafrost soil from Spitsbergen, Northern Norway. Environ Microbiol 9(11):2870–2884. doi:10.1111/j.1462-2920.2007.01403.x
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1–3):1–15. doi:10.1016/j.jhazmat.2009.03.137
Holmfeldt K, Dziallas C, Titelman J, Pohlmann K, Grossart HP, Riemann L (2009) Diversity and abundance of freshwater Actinobacteria along environmental gradients in the brackish northern Baltic Sea. Environ Microbiol 11(8):2042–2054. doi:10.1111/j.1462-2920.2009.01925.x
Hopkins DW, Macnaughton SJ, O’Donnell AG (1991) A dispersion and differentialcentrifugation technique for representatively sampling microorganisms from soil. Soil Biol Biochem 23(3):217–225. doi:10.1016/0038-0717(91)90055-O
Jankowska K, Wlodarska-Kowalczuk M, Wieczorek P (2005) Abundance and biomass of bacteria in two Arctic glacial fjords. Polish Polar Res 26(1):77–84
Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 72(6):3832–3845. doi:10.1128/AEM.02869-05
Kastovska K, Elster J, Stibal M, Santruckova H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (high arctic). Microb Ecol 50(3):396–407. doi:10.1007/s00248-005-0246-4
Khan ST, H`arayama S, Tamura T, Ando K, Takagi M, Kazuo SY (2009) Paraoerskovia marina gen. nov., sp. nov., an actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 59(Pt 8):2094–2098. doi:10.1099/ijs.0.007666-0
Kochkina GA, Ivanushkina NE, Karasev SG, Gavrish EY, Gurina LV, Evtushenko LI, Spirina EV, Vorob’eva EA, Gilichinskii DA, Ozerskaya SM (2001) Survival of Micromycetes and Actinobacteria under conditions of long-term natural cryopreservation. Microbiology 70(3):356–364. doi:10.1023/A:1010419831245
Kurahashi M, Fukunaga Y, Sakiyama Y, Harayama S, Yokota A (2009) Iamia majanohamensis gen. nov., sp. nov., an actinobacterium isolated from sea cucumber Holothuria edulis, and proposal of Iamiaceae fam. nov. Int J Syst Evol Microbiol 59(Pt 4):869–873. doi:10.1099/ijs.0.005611-0
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, pp 115–175
Larose C, Berger S, Ferrari C, Navarro E, Dommergue A, Schneider D, Vogel TM (2010) Microbial sequences retrieved from environmental samples from seasonal arctic snow and meltwater from Svalbard, Norway. Extremophiles 14(2):205–212. doi:10.1007/s00792-009-0299-2
Lazzarini A, Cavaletti L, Toppo G, Marinelli F (2000) Rare genera of actinomycetes as potential producers of new antibiotics. Antonie Van Leeuwenhoek 78(3–4):399–405. doi:10.1023/A:1010287600557
Lee DW, Lee JM, Seo JP, Schumann P, Kim SJ, Lee SD (2008) Phycicola gilvus gen. nov., sp. nov., an actinobacterium isolated from living seaweed. Int J Syst Evol Microbiol 58(Pt 6):1318–1323. doi:10.1099/ijs.0.65283-0
Li HR, Yu Y, Luo W, Zeng YX (2010) Marisediminicola antarctica gen. nov., sp. nov., an actinobacterium isolated from the Antarctic. Int J Syst Evol Microbiol 60(Pt 11):2535–2539. doi:10.1099/ijs.0.018754-0
Lin CL, Tang YL, Lin SM (2011) Efficient bioconversion of compactin to pravastatin by the quinoline-degrading microorganism Pseudonocardia carboxydivorans isolated from petroleum-contaminated soil. Bioresour Technol 102(22):10187–10193. doi:10.1016/j.biortech.2011.09.029
Lysnes K, Thorseth IH, Steinsbu BO, Ovreas L, Torsvik T, Pedersen RB (2004) Microbial community diversity in seafloor basalt from the Arctic spreading ridges. FEMS Microbiol Ecol 50(3):213–230. doi:10.1016/j.femsec.2004.06.014
Maldonado LA, Fenical W, Jensen PR, Kauffman CA, Mincer TJ, Ward AC, Bull AT, Goodfellow M (2005) Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae. Int J Syst Evol Microbiol 55(Pt 5):1759–1766. doi:10.1099/ijs.0.63625-0
Manivasagan P, Venkatesan J, Sivakumar K, Kim SK (2013) Marine actinobacterial metabolites: current status and future perspectives. Microbiol Res 168(6):311–332. doi:10.1016/j.micres.2013.02.002
Mann J (2001) Natural products as immunosuppressive agents. Nat Prod Reports 18(4):417–430. doi:10.1039/B001720P
Mindl B, Anesio AM, Meirer K, Hodson AJ, Laybourn-Parry J, Sommaruga R, Sattler B (2007) Factors influencing bacterial dynamics along a transect from supraglacial runoff to proglacial lakes of a high Arctic glacier [corrected]. FEMS Microbiol Ecol 59(2):307–317. doi:10.1111/j.1574-6941.2006.00262.x
Olano C, Mendez C, Salas JA (2009) Antitumor compounds from marine actinomycetes. Marine Drugs 7(2):210–248. doi:10.3390/md7020210
Padgitt PJ, Moshier SE (1987) Mycobacterium poriferae sp. nov., a scotochromogenic, rapidly growing species isolated from a marine sponge. Int J Syst Bacteriol 37(3):186–191. doi:10.1099/00207713-37-3-186
Park MH, Traiwan J, Jung MY, Kim W (2012) Gulosibacter chungangensis sp. nov., an actinomycete isolated from a marine sediment, and emended description of the genus Gulosibacter. Int J Syst Evol Microbiol 62(Pt 5):1055–1060. doi:10.1099/ijs.0.032268-0
Park SW, Park ST, Lee JE, Kim YM (2008) Pseudonocardia carboxydivorans sp. nov., a carbon monoxide-oxidizing actinomycete, and an emended description of the genus Pseudonocardia. Int J Syst Evol Microbiol 58(Pt 11):2475–2478. doi:10.1099/ijs.0.65765-0
Qin S, Chen HH, Zhao GZ, Li J, Zhu WY, Xu LH, Jiang JH, Li WJ (2012) Abundant and diverse endophytic actinobacteria associated with medicinal plant Maytenus austroyunnanensis in Xishuangbanna tropical rainforest revealed by culture-dependent and culture-independent methods. Environ Microbiol Rep 4(5):522–531. doi:10.1111/j.1758-2229.2012.00357.x
Ramesh S, Mathivanan N (2009) Screening of marine actinomycetes isolated from the Bay of Bengal, India for antimicrobial activity and industrial enzymes. World J Microbiol Biotechnol 25(12):2103–2111. doi:10.1007/s11274-009-0113-4
Ravenschlag K, Sahm K, Amann R (2001) Quantitative molecular analysis of the microbial community in marine arctic sediments (Svalbard). Appl Environ Microbiol 67(1):387–395. doi:10.1128/AEM.67.1.387-395.2001
Rehmann K, Noll HP, Steinberg CE, Kettrup AA (1998) Pyrene degradation by Mycobacterium sp. strain KR2. Chemosphere 36(14):2977–2992. doi:10.1016/S0045-6535(97)10240-5
Riget F, Bignert A, Braune B, Stow J, Wilson S (2010) Temporal trends of legacy POPs in Arctic biota, an update. Sci Total Environ 408(15):2874–2884. doi:10.1016/j.scitotenv.2009.07.036
Sembiring L, Ward AC, Goodfellow M (2000) Selective isolation and characterisation of members of the Streptomyces violaceusniger clade associated with the roots of Paraserianthes falcataria. Antonie Van Leeuwenhoek 78(3–4):353–366. doi:10.1023/A:1010226515202
Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA (2006) Bacterial diversity in three different Antarctic cold desert mineral soils. Microb Ecol 51(4):413–421. doi:10.1007/s00248-006-9022-3
Srinivas TN, Reddy PV, Begum Z, Manasa P, Shivaji S (2012) Oceanisphaera arctica sp. nov., isolated from Arctic marine sediment, and emended description of the genus Oceanisphaera. Int J Syst Evol Microbiol 62(Pt 8):1926–1931. doi:10.1099/ijs.0.036475-0
Stach JE, Maldonado LA, Ward AC, Goodfellow M, Bull AT (2003) New primers for the class Actinobacteria: application to marine and terrestrial environments. Environ Microbiol 5(10):828–841. doi:10.1046/j.1462-2920.2003.00483.x
Sun W, Dai S, Jiang S, Wang G, Liu G, Wu H, Li X (2010) Culture-dependent and culture-independent diversity of Actinobacteria associated with the marine sponge Hymeniacidon perleve from the South China Sea. Antonie Van Leeuwenhoek 98(1):65–75. doi:10.1007/s10482-010-9430-8
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121
Teng H, Tang H, Xiao H, Shu Y, Li H (2009) Isolation and identification of actinobacteria from Rhizospheric soil in the Arctic Yellow river station. Advances Polar Sci 21(1):33–42. doi:CNKI:SUN:JDYZ.0.2009-01-005
Tian XP, Tang SK, Dong JD, Zhang YQ, Xu LH, Zhang S, Li WJ (2009a) Marinactinospora thermotolerans gen. nov., sp. nov., a marine actinomycete isolated from a sediment in the northern South China Sea. Int J Syst Evol Microbiol 59(Pt 5):948–952. doi:10.1099/ijs.0.005231-0
Tian XP, Zhi XY, Qiu YQ, Zhang YQ, Tang SK, Xu LH, Zhang S, Li WJ (2009b) Sciscionella marina gen. nov., sp. nov., a marine actinomycete isolated from a sediment in the northern South China Sea. Int J Syst Evol Microbiol 59(Pt 2):222–228. doi:10.1099/ijs.0.001982-0
Tsukamura M, Nemoto H, Yugi H (1983) Mycobacterium porcinum sp. nov., a Porcine pathogen. Int J Syst Bacteriol 33(2):162–165. doi:10.1099/00207713-33-2-162
Ue H, Matsuo Y, Kasai H, Yokota A (2011) Miniimonas arenae gen. nov., sp. nov., an actinobacterium isolated from sea sand. Int J Syst Evol Microbiol 61(Pt 1):123–127. doi:10.1099/ijs.0.019596-0
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. doi:10.1128/AEM.00062-07
Ward AC, Bora N (2006) Diversity and biogeography of marine actinobacteria. Curr Opin Microbiol 9(3):279–286. doi:10.1016/j.mib.2006.04.004
Watanapokasin Y, Nuchfoang S, Nilwarangkoon S, Sarangbin S, Kakizono T (2002) Isolation and characterization of thermophilic benzothiophene-degrading Mycobacterium sp. Appl Biochem Biotechnol 98–100:301–309. doi:10.1007/978-1-4612-0119-9_24
Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78(3):717–725. doi:10.1128/AEM.06516-11
Xiao J, Luo Y, Xu J, Xie S (2011) Modestobacter marinus sp. nov., a psychrotolerant actinobacterium from deep-sea sediment, and emended description of the genus Modestobacter. Int J Syst Evol Microbiol 61(7):1710–1714. doi:10.1099/ijs.0.023085-0
Yi H, Schumann P, Chun J (2007) Demequina aestuarii gen. nov., sp. nov., a novel actinomycete of the suborder Micrococcineae, and reclassification of Cellulomonas fermentans Bagnara et al. 1985 as Actinotalea fermentans gen. nov., comb. nov. Int J Syst Evol Microbiol 57(Pt 1):151–156. doi:10.1099/ijs.0.64525-0
Yi H, Schumann P, Sohn K, Chun J (2004) Serinicoccus marinus gen. nov., sp. nov., a novel actinomycete with l-ornithine and l-serine in the peptidoglycan. Int J Syst Evol Microbiol 54(Pt 5):1585–1589. doi:10.1099/ijs.0.03036-0
Acknowledgments
This work was supported by grants from the Scientific Research Foundation of Third Institute of Oceanography (2011002), COMRA program (No. DY125-15-R-01), National Natural Science Foundation of China (41206160) and China Polar Environment Investigation and Estimate Project (CHINARE2012-2015).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, G., Cao, T., Ying, J. et al. Diversity and novelty of actinobacteria in Arctic marine sediments. Antonie van Leeuwenhoek 105, 743–754 (2014). https://doi.org/10.1007/s10482-014-0130-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-014-0130-7