Hunting for pigments in bacterial settlers of the Great Pacific Garbage Patch.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
Jun 2024
Jun 2024
Historique:
received:
07
07
2023
accepted:
30
04
2024
medline:
20
6
2024
pubmed:
20
6
2024
entrez:
20
6
2024
Statut:
ppublish
Résumé
The Great Pacific Garbage Patch, a significant collection of plastic introduced by human activities, provides an ideal environment to study bacterial lifestyles on plastic substrates. We proposed that bacteria colonizing the floating plastic debris would develop strategies to deal with the ultraviolet-exposed substrate, such as the production of antioxidant pigments. We observed a variety of pigmentation in 67 strains that were directly cultivated from plastic pieces sampled from the Garbage Patch. The genomic analysis of four representative strains, each distinct in taxonomy, revealed multiple pathways for carotenoid production. These pathways include those that produce less common carotenoids and a cluster of photosynthetic genes. This cluster appears to originate from a potentially new species of the Rhodobacteraceae family. This represents the first report of an aerobic anoxygenic photoheterotrophic bacterium from plastic biofilms. Spectral analysis showed that the bacteria actively produce carotenoids, such as beta-carotene and beta-cryptoxanthin, and bacteriochlorophyll a. Furthermore, we discovered that the genetic ability to synthesize carotenoids is more common in plastic biofilms than in the surrounding water communities. Our findings suggest that plastic biofilms could be an overlooked source of bacteria-produced carotenoids, including rare forms. It also suggests that photoreactive molecules might play a crucial role in bacterial biofilm communities in surface water.
Identifiants
pubmed: 38899733
doi: 10.1111/1462-2920.16639
doi:
Substances chimiques
Carotenoids
36-88-4
Pigments, Biological
0
Plastics
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e16639Subventions
Organisme : Bundesministerium für Bildung und Forschung
ID : 03G0268TA
Organisme : Bundesministerium für Bildung und Forschung
ID : 03G0268TC
Informations de copyright
© 2024 The Authors. Environmental Microbiology published by John Wiley & Sons Ltd.
Références
Akulava, V., Byrtusova, D., Zimmermann, B., Smirnova, M., Kohler, A., Miamin, U. et al. (2024) Screening for pigment production and characterization of pigment profile and photostability in cold‐adapted Antarctic bacteria using FT‐Raman spectroscopy. Journal of Photochemistry and Photobiology. A, Chemistry, 450, 115461.
Altschul, S.F. & Gish, W. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.
Amaral‐Zettler, L.A. & Zettler, E.R. (2015) The biogeography of the Plastisphere: implications for policy. Frontiers in Ecology and the Environment, 13, 541–546. Available from: https://doi.org/10.1890/150017
Amaral‐Zettler, L.A., Zettler, E.R. & Mincer, T.J. (2020) Ecology of the plastisphere. Nature Reviews. Microbiology, 18(3), 139–151.
Anderson, M.J. (2001) A new method for non‐parametric multivariate analysis of variance. Austral Ecology, 26, 32–46. Available from: https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Anderson, M.J. (2017) Permutational multivariate analysis of variance (PERMANOVA). In: Balakrishnan, N., Colton, T., Everitt, B., Piegorsch, W., Ruggeri, F. & Teugels, J.L. (Eds.) Wiley statsref: statistics reference online. John Wiley & Sons. Available from: https://doi.org/10.1002/9781118445112.stat07841
Andrews, S., Krueger, F., Segonds‐Pichon, A., Biggins, L., Krueger, C. & Wingett, S. (2010) FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics. Available at: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Aramaki, T. & Blanc‐Mathieu, R. (2020) KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics, 36(7), 2251–2252.
Ashikhmin, A. et al. (2017) Incorporation of spheroidene and spheroidenone into light‐harvesting complexes from purple sulfur bacteria. Journal of Photochemistry and Photobiology. B, Biology, 170, 99–107.
Auch, A.F. & von Jan, M. (2010) Digital DNA‐DNA hybridization for microbial species delineation by means of genome‐to‐genome sequence comparison. Standards in Genomic Sciences, 2(1), 117–134.
Azai, C. et al. (2020) Anaerobic energy dissipation by glycosylated carotenoids in the green sulfur bacterium Chlorobaculum tepidum. Journal of Photochemistry and Photobiology. A, Chemistry, 403, 112828.
Basili, M., Quero, G.M., Giovannelli, D., Manini, E., Vignaroli, C., Avio, C.G. et al. (2020) Major role of surrounding environment in shaping biofilm community composition on marine plastic debris. Frontiers in Marine Science, 7, 525550. Available from: https://doi.org/10.3389/fmars.2020.00262
Beaz‐Hidalgo, R. & Balboa, S. (2010) Diversity and pathogenecity of vibrio species in cultured bivalve molluscs. Environmental Microbiology Reports, 2(1), 34–43.
Biebl, H. & Pukall, R. (2007) Description of Labrenzia alexandrii gen. nov., sp. nov., a novel alphaproteobacterium containing bacteriochlorophyll a, and a proposal for reclassification of Stappia aggregata as Labrenzia aggregata comb. nov., of Stappia marina as Labrenzia marina comb. nov. and of Stappia alba as Labrenzia alba comb. nov., and emended descriptions of the genera Pannonibacter, Stappia and Roseibium, and of the species Roseibium denhamense and Roseibium hamelinense. International Journal of Systematic and Evolutionary Microbiology, 57(Pt 5), 1095–1107.
Biller, S.J., Berube, P.M., Dooley, K., Williams, M., Satinsky, B.M., Hackl, T. et al. (2018) Marine microbial metagenomes sampled across space and time. Scientific Data, 5, 180176.
Blin, K. & Shaw, S. (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Research, 49(W1), W29–W35.
Bolyen, E. & Rideout, J.R. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8), 852–857.
Bos, R.P. & Kaul, D. (2023) Plastics select for distinct early colonizing microbial populations with reproducible traits across environmental gradients. Environmental Microbiology, 25(12), 2761–2775.
Brady, C.L. & Venter, S.N. (2009) Pantoea vagans sp. nov., Pantoea eucalypti sp. nov., Pantoea deleyi sp. nov. and Pantoea anthophila sp. nov. International Journal of Systematic and Evolutionary Microbiology, 59(Pt 9), 2339–2345.
Brinkmann, H. & Göker, M. (2018) Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae. The ISME Journal, 12(8), 1994–2010.
Bryant, J.A., Clemente, T.M., Viviani, D.A., Fong, A.A., Thomas, K.A., Kemp, P. et al. (2016) Diversity and activity of communities inhabiting plastic debris in the North Pacific Gyre. MSystems, 1. Available from: https://doi.org/10.1128/mSystems.00024-16
Bushnell, B. (2014) BBMap, SOURCEFORGE. Available at: https://sourceforge.net/projects/bbmap/
Callahan, B.J. & McMurdie, P.J. (2016) DADA2: high‐resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581–583.
Chaumeil, P.‐A. & Mussig, A.J. (2019) GTDB‐Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics, 36(6), 1925–1927.
Chong, F. & Spencer, M. (2023) High concentrations of floating neustonic life in the plastic‐rich North Pacific garbage patch. PLoS Biology, 21(5), e3001646.
Cogdell, R.J. et al. (2000) How carotenoids protect bacterial photosynthesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 355(1402), 1345–1349.
Dieser, M., Greenwood, M. & Foreman, C.M. (2010) Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arctic, Antarctic, and Alpine Research, 42(4), 396–405.
Eriksen, M., Lebreton, L.C.M., Carson, H.S., Thiel, M., Moore, C.J., Borerro, J.C. et al. (2014) Plastic pollution in the world's oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PloS One, 9(12), e111913.
Frank, J.A. & Reich, C.I. (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Applied and Environmental Microbiology, 74(8), 2461–2470.
Geyer, R., Jambeck, J.R. & Law, K.L. (2017) Production, use, and fate of all plastics ever made. Science Advances, 3(7), e1700782.
Goericke, R. (2002) Bacteriochlorophyllain the ocean: is anoxygenic bacterial photosynthesis important? Limnology and Oceanography, 47(1), 290–295.
Hallgren, J. et al. (2022) ‘DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks’, bioRxiv. https://doi.org/10.1101/2022.04.08.487609
Haram, L.E., Carlton, J.T., Centurioni, L., Crowley, M., Hafner, J., Maximenko, N. et al. (2021) Emergence of a neopelagic community through the establishment of coastal species on the high seas. Nature Communications, 12(1), 6885.
Hauruseu, D. & Koblížek, M. (2012) Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Applied and Environmental Microbiology, 78(20), 7414–7419.
Higgins, B.P., Carpenter, C.D. & Karls, A.C. (2007) Chromosomal context directs high‐frequency precise excision of IS492 in Pseudoalteromonas atlantica. Proceedings of the National Academy of Sciences of the United States of America, 104(6), 1901–1906.
Hyatt, D. & Chen, G.L. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11, 119.
Jain, C. & Rodriguez‐R, L.M. (2018) High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications, 9(1), 5114.
Jambeck, J.R., Geyer, R., Wilcox, C., Siegler, T.R., Perryman, M., Andrady, A. et al. (2015) Plastic waste inputs from land into the ocean. Science, 347(6223), 768–771.
Jiang, L. & Seo, J. (2023) A nostoxanthin‐producing bacterium, Sphingomonas nostoxanthinifaciens sp. nov., alleviates the salt stress of Arabidopsis seedlings by scavenging of reactive oxygen species. Frontiers in Microbiology, 14, 1101150.
Jones, P. & Binns, D. (2014) InterProScan 5: genome‐scale protein function classification. Bioinformatics, 30(9), 1236–1240.
Kanehisa, M. & Goto, S. (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Research, 28(1), 27–30.
Katoh, K. & Misawa, K. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059–3066.
Kesy, K. & Labrenz, M. (2020) Vibrio colonization is highly dynamic in early microplastic‐associated biofilms as well as on field‐collected microplastics. Microorganisms, 9(1), 76. Available from: https://doi.org/10.3390/microorganisms9010076
Kesy, K. & Oberbeckmann, S. (2019) Spatial environmental heterogeneity determines young biofilm assemblages on microplastics in Baltic Sea Mesocosms. Frontiers in Microbiology, 10, 1665.
Kikukawa, H., Okaya, T., Maoka, T., Miyazaki, M., Murofushi, K., Kato, T. et al. (2021) Carotenoid nostoxanthin production by Sphingomonas sp. SG73 Isolated from Deep Sea Sediment. Marine Drugs, 19(5), 274. Available from: https://doi.org/10.3390/md19050274
Koblížek, M. (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiology Reviews, 39(6), 854–870.
Kolmogorov, M. & Yuan, J. (2019) Assembly of long, error‐prone reads using repeat graphs. Nature Biotechnology, 37(5), 540–546.
Kurahashi, M. & Yokota, A. (2007) Tateyamaria omphalii gen. Nov., sp. nov., an alpha‐Proteobacterium isolated from a top shell Omphalius pfeifferi pfeifferi. Systematic and Applied Microbiology, 30(5), 371–375.
Lebreton, L., Slat, B., Ferrari, F., Sainte‐Rose, B., Aitken, J., Marthouse, R. et al. (2018) Evidence that the great pacific garbage patch is rapidly accumulating plastic. Scientific Reports, 8(1), 4666.
Li, H. (2013) ‘Aligning sequence reads, clone sequences and assembly contigs with BWA‐MEM’, arXiv [q‐bio.GN]. Available at: http://arxiv.org/abs/1303.3997
Liao, Y., Smyth, G.K. & Shi, W. (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30(7), 923–930.
Liu, Y. & Pei, T. (2022) Comparative genomics reveals genetic diversity and metabolic potentials of the genus Qipengyuania and suggests fifteen novel species. Microbiology Spectrum, 10(3), e0126421.
MacLeod, M. & Arp, H.P.H. (2021) The global threat from plastic pollution. Science, 373(6550), 61–65.
Mao, D.‐P. & Zhou, Q. (2012) Coverage evaluation of universal bacterial primers using the metagenomic datasets. BMC Microbiology, 12, 66.
Meléndez‐Martínez, A.J. & Mapelli‐Brahm, P. (2015) A comprehensive review on the colorless carotenoids phytoene and phytofluene. Archives of Biochemistry and Biophysics, 572, 188–200.
Mendes‐Silva, T.D.C.D., Vidal, E.E., de Souza, R.D.F.R., da Cunha Schmidt, K., Mendes, P.V.D., da Silva Andrade, R.F. et al. (2021) Production of carotenoid sarcinaxanthin by Kocuria palustris isolated from Northeastern Brazil Caatinga soil and their antioxidant and photoprotective activities. Electronic Journal of Biotechnology: EJB, 53, 44–53.
Niedzwiedzki, D.M. & Dilbeck, P.L. (2015) Functional characteristics of spirilloxanthin and keto‐bearing analogues in light‐harvesting LH2 complexes from Rhodobacter sphaeroides with a genetically modified carotenoid synthesis pathway. Biochimica et Biophysica Acta, 2015(6‐7), 640–655.
Oberbeckmann, S., Bartosik, D., Huang, S., Werner, J., Hirschfeld, C., Wibberg, D. et al. (2021) Genomic and proteomic profiles of biofilms on microplastics are decoupled from artificial surface properties. Environmental Microbiology, 23(6), 3099–3115.
Osawa, A. & Ishii, Y. (2010) Characterization and antioxidative activities of rare C(50) carotenoids‐sarcinaxanthin, sarcinaxanthin monoglucoside, and sarcinaxanthin diglucoside‐obtained from Micrococcus yunnanensis. Journal of Oleo Science, 59(12), 653–659.
Paoli, L., Ruscheweyh, H.‐J., Forneris, C.C., Hubrich, F., Kautsar, S., Bhushan, A. et al. (2022) Biosynthetic potential of the global ocean microbiome. Nature, 607(7917), 111–118.
Piwosz, K., Villena‐Alemany, C. & Mujakić, I. (2022) Photoheterotrophy by aerobic anoxygenic bacteria modulates carbon fluxes in a freshwater lake. The ISME Journal, 16(4), 1046–1054.
Prjibelski, A. & Antipov, D. (2020) Using SPAdes De Novo Assembler. Current Protocols in Bioinformatics, 70(1), e102.
Pujalte, M.J. & Lucena, T. (2014) The family Rhodobacteraceae. In: The prokaryotes. Berlin: Springer, pp. 439–512.
Ram, S. & Mitra, M. (2020) Bacteria as an alternate biofactory for carotenoid production: a review of its applications, opportunities and challenges. Journal of Functional Foods, 67, 103867.
Roman, N. et al. (2010) Biosynthetic pathway for γ‐cyclic Sarcinaxanthin in Micrococcus luteus: heterologous expression and evidence for diverse and multiple catalytic functions of C50 carotenoid cyclases. Journal of Bacteriology, 192(21), 5688–5699.
Ruivo, M. & Cartaxana, P. (2014) Extraction and quantification of pigments in aerobic anoxygenic phototrophic bacteria. Limnology and Oceanography: Methods, 12(6), 338–350.
Rynek, R. & Tekman, M.B. (2024) Hotspots of floating plastic particles across the North Pacific Ocean. Environmental Science & Technology, 58(9), 4302–4313.
Salazar, G., Paoli, L., Alberti, A., Huerta‐Cepas, J., Ruscheweyh, H.‐J., Cuenca, M. et al. (2019) Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell, 179(5), 1068–1083.e21.
Sandmann, G. (2023) Genes and pathway reactions related to carotenoid biosynthesis in purple bacteria. Biology, 12(10), 1346. Available from: https://doi.org/10.3390/biology12101346
Sawabe, T. & Tanaka, R. (2000) Assignment of Alteromonas elyakovii KMM 162T and five strains isolated from spot‐wounded fronds of Laminaria japonica to Pseudoalteromonas elyakovii comb. nov. and the extended description of the species. International Journal of Systematic and Evolutionary Microbiology, 50, 265–271. Available from: https://doi.org/10.1099/00207713-50-1-265
Scales, B.S., Cable, R.N., Duhaime, M.B., Gerdts, G., Fischer, F., Fischer, D. et al. (2021) Cross‐hemisphere study reveals geographically ubiquitous, plastic‐specific bacteria emerging from the rare and unexplored biosphere. MSphere, 6(3), e0085120.
Seemann, T. (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics, 30(14), 2068–2069.
Shen, W. & Le, S. (2016) SeqKit: a cross‐platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS One, 11(10), e0163962.
Simidu, U. et al. (1990) Taxonomy of four marine bacterial strains that produce tetrodotoxin. International Journal of Systematic Bacteriology, 40(4), 331–336.
Šlouf, V. & Chábera, P. (2012) Photoprotection in a purple phototrophic bacterium mediated by oxygen‐dependent alteration of carotenoid excited‐state properties. Proceedings of the National Academy of Sciences of the United States of America, 109(22), 8570–8575.
Steen, A.D. & Crits‐Christoph, A. (2019) High proportions of bacteria and archaea across most biomes remain uncultured. The ISME Journal, 13, 3126–3130.
Takano, H. & Asker, D. (2006) Genetic control for light‐induced carotenoid production in non‐phototrophic bacteria. Journal of Industrial Microbiology & Biotechnology, 33(2), 88–93.
Tareen, S. & Risdian, C. (2022) Qipengyuania pacifica sp. nov., a novel carotenoid‐producing marine bacterium of the family Erythrobacteraceae, isolated from sponge (Demospongiae), and antimicrobial potential of its crude extract. Diversity, 14(4), 295.
Thijs, S. et al. (2017) Comparative evaluation of four bacteria‐specific primer pairs for 16S rRNA gene surveys. Frontiers in Microbiology, 8, 494.
Uritskiy, G.V., DiRuggiero, J. & Taylor, J. (2018) MetaWRAP—a flexible pipeline for genome‐resolved metagenomic data analysis. Microbiome, 6(1), 158.
Vaksmaa, A., Knittel, K., Abdala Asbun, A., Goudriaan, M., Ellrott, A., Witte, H.J. et al. (2021) Microbial communities on plastic polymers in the Mediterranean sea. Frontiers in Microbiology, 12, 673553.
Walker, B.J. & Abeel, T. (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One, 9(11), e112963.
Yabuzaki, J. (2017) Carotenoids database: structures, chemical fingerprints and distribution among organisms. Database: The Journal of Biological Databases and Curation, 2017(1), 2016. Available from: https://doi.org/10.1093/database/bax004
Yoon, S.‐H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H. et al. (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole‐genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67(5), 1613–1617.
Zachariah, S., Kumari, P. & Das, S.K. (2016) Psychrobacter pocilloporae sp. nov., isolated from a coral, Pocillopora eydouxi. International Journal of Systematic and Evolutionary Microbiology, 66(12), 5091–5098.