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Conserved Pigment Profiles in Phylogenetically Diverse Symbiotic Bacteria Associated with the Corals Montastraea cavernosa and Mussismilia braziliensis

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Abstract

Pigmented bacterial symbionts play major roles in the health of coral holobionts. However, there is scarce knowledge on the diversity of these microbes for several coral species. To gain further insights into holobiont health, pigmented bacterial isolates of Fabibacter pacificus (Bacteroidetes; n = 4), Paracoccus marcusii (Alphaproteobacteria; n = 1), and Pseudoalteromonas shioyasakiensis (Gammaproteobacteria; n = 1) were obtained from the corals Mussismilia braziliensis and Montastraea cavernosa in Abrolhos Bank, Brazil. Cultures of these bacterial symbionts produced strong antioxidant activity (catalase, peroxidase, and oxidase). To explore these bacterial isolates further, we identified their major pigments by HPLC and mass spectrometry. The six phylogenetically diverse symbionts had similar pigment patterns and produced myxol and keto-carotene. In addition, similar carotenoid gene clusters were confirmed in the whole genome sequences of these symbionts, which reinforce their antioxidant potential. This study highlights the possible roles of bacterial symbionts in Montastraea and Mussismilia holobionts.

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References

  1. Bourne DG, Morrow KM, Webster NS (2016) Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems. Insights into the coral. Underpinning the Health and Resilience of Reef Ecosystems. Annual Review of Microbiology, Microbiome. https://doi.org/10.1146/annurev-micro-102215-095440

  2. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362. https://doi.org/10.1038/nrmicro1635

    Article  CAS  PubMed  Google Scholar 

  3. Silveira CB, Cavalcanti GS, Walter JM, Silva-Lima AW, Dinsdale EA, Bourne DG, Thompson CC, Thompson FL (2017a) Microbial processes driving coral reef organic carbon flow. FEMS Microbiol Rev 41:575–595. https://doi.org/10.1093/femsre/fux018

    Article  CAS  PubMed  Google Scholar 

  4. Roth MS (2014) The engine of the reef: photobiology of the coral–algal symbiosis. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00422

  5. Wooldridge SA (2013) Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences 10:1647–1658. https://doi.org/10.5194/bg-10-1647-2013

    Article  Google Scholar 

  6. Gierz SL, Forêt S, Leggat W (2017) Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00271

  7. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. Exp Biol 211:3059–3066. https://doi.org/10.1242/jeb.009597

    Article  CAS  Google Scholar 

  8. Motone K, Takagi T, Aburaya S, Miura N, Aoki W, Ueda M (2020) A zeaxanthin-producing bacterium isolated from the algal phycosphere protects coral endosymbionts from environmental stress. mBio. https://doi.org/10.1128/mBio.01019-19

  9. Shindo K, Kikuta K, Suzuki A, Katsuta A, Kasai H, Yasumoto-Hirose M, Matsuo Y, Misawa N, Takaichi S (2007) Rare carotenoids, (3R)-saproxanthin and (3R, 2′ S)-myxol, isolated from novel marine bacteria (Flavobacteriaceae) and their antioxidative activities. Appl Microbiol Biotechnol 74:1350–1357. https://doi.org/10.1007/s00253-006-0774-y

    Article  CAS  PubMed  Google Scholar 

  10. Havaux M, Dall’osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520. https://doi.org/10.1104/pp.107.108480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci. https://doi.org/10.1016/S1360-1385(98)01200-X

  12. Hoegh-Guldberg O, Jacob D, Taylor M, Bindi M, Brown S, Camilloni I, Diedhiou A, Djalante R, Ebi K, Engelbrecht F, Guiot J, et al (2018) Impacts of 1.5 °C global warming on natural and human systems. https://www.ipcc.ch/site/assets/uploads/sites/2/2018/12/SR15

  13. De Castro AP, Araújo SD, Reis AM, Moura RL, Francini-Filho RB, Pappas G, Rodrigues TB, Thompson FL, Krüger RH (2010) Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from eastern Brazil. Microb Ecol 59:658–667. https://doi.org/10.1007/s00248-010-9646-1

    Article  PubMed  Google Scholar 

  14. Fernando SC, Wang J, Sparling K, Garcia GD, Francini-Filho RB, de Moura RL, Paranhos R, Thompson FL, Thompson JR (2015) Microbiota of the major South Atlantic reef building coral Mussismilia. Microb Ecol 69:267–280. https://doi.org/10.1007/s00248-014-0474-6

    Article  PubMed  Google Scholar 

  15. Reis AAM, Araújo JRS, Moura R, Francini-Filho R, Pappas JRG, Coelho A, Krüger R, Thompson F (2009) Bacterial diversity asso- ciated with the Brazilian endemic reef coral Mussismilia braziliensis. J Appl Microbiol 106:1378–1387. https://doi.org/10.1111/j.1365-2672.2008.04106.x

    Article  CAS  PubMed  Google Scholar 

  16. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10. https://doi.org/10.3354/meps243001

    Article  Google Scholar 

  17. Silveira CB, Gregoracci GB, Coutinho FH, Silva GG, Haggerty JM, de Oliveira LS, Cabral AS, Rezende CE, Thompson CC, Francini-Filho RB (2017b) Bacterial community associated with the reef coral Mussismilia braziliensis's momentum boundary layer over a diel cycle. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.00784

  18. Walsh K, Haggerty JM, Doane MP, Hansen JJ, Morris MM, Moreira APB, de Oliveira L, Leomil L, Garcia GD, Thompson F (2017) Aura-biomes are present in the water layer above coral reef benthic macro-organisms. Peer J 5:e3666. https://doi.org/10.7717/peerj.3666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Silva-Lima AW, Walter JM, Garcia GD, Ramires N, Ank G, Meirelles PM, Nobrega AF, Siva-Neto ID, Moura RL, Salomon PS, Thompson CC, Thompson FL (2015) Multiple Symbiodinium strains are hosted by the Brazilian endemic corals Mussismilia spp. Microb Ecol 70:301–310. https://doi.org/10.1007/s00248-015-0573-z

    Article  PubMed  Google Scholar 

  20. Reiner K (2010) Catalase test protocol. American society for microbiology

  21. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864. https://doi.org/10.1093/bioinformatics/btr026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Coil D, Jospin G, Darling AE (2014) A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 31:587–589. https://doi.org/10.1093/bioinformatics/btu661

    Article  CAS  PubMed  Google Scholar 

  23. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877. https://doi.org/10.1101/gr.9.9.868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Moreira APB, Duytschaever G, Tonon LAC, Dias GM, Mesquita M, Cnockaert M, Francini-Filho RB, De Vos P, Thompson CC, Thompson FL (2014) Vibrio madracius sp. nov. isolated from Madracis decactis (Scleractinia) in St Peter & St Paul Archipelago, Mid-Atlantic Ridge, Brazil. Curr Microbiol. https://doi.org/10.1007/s00284-014-0600-1

  25. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Saitou N, Nei M (1987) The neighbor-joiningmethod: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  27. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  28. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  29. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HH (ed) Mammalian protein metabolism. Academic Press, London, pp 21–132. https://doi.org/10.1016/B978-1-4832-3211-9.50009-7

    Chapter  Google Scholar 

  30. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16. https://doi.org/10.1093/nar/gkh152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Medema MH, Blin K, Cimermancic P, Jager V, Zakrzewski P, Fischbach MA, Breitling R (2011) antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39:W339–W346. https://doi.org/10.1093/nar/gkr466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lombard V, GolacondaRamulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495. https://doi.org/10.1093/nar/gkt1178

    Article  CAS  PubMed  Google Scholar 

  35. Rawlings ND, Barrett AJ, Thomas PD, Huang X, Bateman A, Finn RD (2018) The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Res 46:D624–D632. https://doi.org/10.1093/nar/gkx1134

    Article  CAS  PubMed  Google Scholar 

  36. Tao L, Yao H, Kasai H, Misawa N, Cheng Q (2006) A carotenoid synthesis gene cluster from Algoriphagus sp. KK10202C with a novel fusion-type lycopene β-cyclase gene. Mol Gen Genomics. https://doi.org/10.1007/s00438-006-0121-0

  37. Schwieter U, Bolliger HR, Chopart-dit-Jean LH, Englert G, Kofler M, Av K, Planta G, Ruegg R, Vetter W, Isler O (1965) Synthesen in der Carotinoid-Reihe. Chimia 19:294–302

    CAS  Google Scholar 

  38. Van Breemen RB, Schmitz HH, Schwartz SJ (1995) Fast atom bombardment tandem mass spectrometry of carotenoids. J Agric Food Chem 43:384–389

    Article  Google Scholar 

  39. Dembitsky VM (2005) Astonishing diversity of natural surfactants. 3. Carotenoid glycosides and isoprenoid glycolipids. Lipids 40:535–557. https://doi.org/10.1007/s11745-005-1415-z

    Article  CAS  PubMed  Google Scholar 

  40. Llewellyn CA, Airs RL, Farnham G, Greig C (2020) Synthesis, regulation and degradation of carotenoids under low level UV-B radiation in the filamentous Cyanobacterium Chlorogloeopsis fritschii. Front Microbiol 11:163. https://doi.org/10.3389/fmicb.2020.00163

    Article  PubMed  PubMed Central  Google Scholar 

  41. Rivera SM, Christou P, Canela-Garayoam R (2014) Identification of carotenoids using mass spectrometry. Mass Spectrom Rev 33:353–372. https://doi.org/10.1002/mas.21390

    Article  CAS  PubMed  Google Scholar 

  42. Britton G, Liaaen-Jensen S, Pfander H (2004) Handbook of carotenoids. Basel, Birkhauser-Verlag

    Book  Google Scholar 

  43. Yokoyama A, Miki W (1995) Isolation of myxol from a marine bacterium Flavobacterium sp. associated with a marine sponge. Fish Sci. https://doi.org/10.2331/fishsci.61.684

  44. Liaaen-Jensen S (1978b) Marine carotenoids. In: Falkner DJ, Fenical WH (eds) Marine Natural Products. Academic Press, pp l–73

  45. Tsubokura A, Yoneda H, Mizuta H (1999) Paracoccus carotinifaciens sp. nov., a new aerobic gram-negative astaxanthin-producing bacterium. Int J Syst Evol Microbiol 49(1):277–282. https://doi.org/10.1099/00207713-49-1-277

    Article  CAS  Google Scholar 

  46. Hudson J, Kumar V, Egan S (2019) Comparative genome analysis provides novel insight into the interaction of Aquimarina sp. AD1, BL5 and AD10 with their macroalgal host. Mar Genomics. https://doi.org/10.1016/j.margen.2019.02.005

  47. Si YY, Xu KH, Yu XY, Wang MF, Chen XH (2019) Complete genome sequence of Paracoccus denitrificans ATCC 19367 and its denitrification characteristics. Can J Microbiol 65:486–495. https://doi.org/10.1139/cjm-2019-0037

    Article  CAS  PubMed  Google Scholar 

  48. Varasteh T, Moreira APB, Lima AWS, Leomil L, Otsuki K, Tschoeke D, Garcia G, Thompson C, Thompson F (2019) Genomic repertoire of Mameliella alba Ep20 associated with Symbiodinium from the endemic coral Mussismilia braziliensis. Symbiosis 80:53–60. https://doi.org/10.1007/s13199-019-00655-x

    Article  CAS  Google Scholar 

  49. Cooper MB, Smith AG (2015) Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr Opin Plant Biol 26:147–153. https://doi.org/10.1016/j.pbi.2015.07.003

    Article  PubMed  Google Scholar 

  50. Amin S, Hmelo L, Van TH, Durham B, Carlson L, Heal K, Morales R, Berthiaume C, Parker M, Djunaedi B (2015) Interaction and signaling between a cosmopolitan phytoplankton and associated bacteria. Nature. 522:98–101. https://doi.org/10.1038/nature14488

    Article  CAS  PubMed  Google Scholar 

  51. Franks A, Haywood P, HolmströmC ES, Kjelleberg S, Kumar N (2005) Isolation and structure elucidation of a novel yellow pigment from the marine bacterium Pseudoalteromonas tunicata. Molecules 10(10):1286–1291. https://doi.org/10.3390/10101286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lau SC, Tsoi MM, Li X, Plakhotnikova I, Dobretsov S, Wu M, Qian PY (2006) Description of Fabibacter halotolerans gen. Nov., sp. and Roseivirga spongicola sp. nov., and reclassification of [Marinicola] seohaensis as Roseivirga seohaensis comb. nov. Int J Syst Evol Microbiol 56(5):1059–1065. https://doi.org/10.1099/ijs.0.64104-0

    Article  CAS  PubMed  Google Scholar 

  53. Misawa N, Satomi Y, Kondo K, Yokoyama A, Kajiwara S, Saito T, Miki W (1995) Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol 177:6575–6584. https://doi.org/10.1128/jb.177.22.6575-6584.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Choi DH, Cho BC (2006) Lutibacter litoralis gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from tidal flat sediment. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijs.0.64146-0

  55. Teramoto M, Rählert N, Misawa N, Sandmann G (2004) 1-Hydroxymonocyclic carotenoid 3, 4-dehydrogenase froma marine bacterium that produces myxol. FEBS Lett 570:184–188. https://doi.org/10.1016/j.febslet.2004.05.085

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful for the support offered by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Pesquisas (CNPq), and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

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Funding

Support offered by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Pesquisas (CNPq), and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

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Authors and Affiliations

  1. Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, RJ, 21941-599, Brazil

    Tooba Varasteh, Diogo Tschoeke, Arthur Silva Lima, Gizele Garcia, Cristiane Thompson & Fabiano Thompson

  2. Instituto de Pesquisas de Produtos Naturais, Federal University of Rio de Janeiro, Rio de Janeiro, RJ, 21941-902, Brazil

    Lidilhone Hamerski

  3. Departamento de Ensino de Graduação, Universidade Federal do Rio de Janeiro - Campus UFRJ - Macaé Professor Aloisio Teixeira, Macaé, Rio de Janeiro, RJ, 27930-480, Brazil

    Gizele Garcia

  4. SAGE - COPPE, Centro de Gestão Tecnológica - CT2, Rio de Janeiro, RJ, Brazil

    Carlos Alberto Nunes Cosenza & Fabiano Thompson

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  1. Tooba Varasteh
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  8. Fabiano Thompson
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Contributions

Tooba Varasteh conceived the study design, bacterial pigment extractions, bacterial DNA extractions, the bioinformatics analysis, and discussion of the results and drafted the manuscript.

Lidilhone Hamerski performed the pigment analyses and participated in the discussion of the results.

Diogo Tschoeke, Arthur Silva Lima, Gizele Garcia, Carlos Alberto Nunes Cosenza, and Cristiane Thompson participated in the discussion of the results and drafted manuscript.

Fabiano Lopes Thompson participated in the acquisition of funding and conceived the study design, discussion of the results, and draft of the manuscript.

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Correspondence to Fabiano Thompson.

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Varasteh, T., Hamerski, L., Tschoeke, D. et al. Conserved Pigment Profiles in Phylogenetically Diverse Symbiotic Bacteria Associated with the Corals Montastraea cavernosa and Mussismilia braziliensis. Microb Ecol 81, 267–277 (2021). https://doi.org/10.1007/s00248-020-01551-4

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