Characterization of planktonic and biofilm cells from two filamentous cyanobacteria using a shotgun proteomic approach

References

• Alexova R, Haynes PA, Ferrari BC, Neilan BA. 2011. Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa. Mol Cell Proteom. 10:M110.003749. doi:10.1074/mcp.M110.003749
   PubMed Web of Science ®Google Scholar
• Allen AA, Habimana O, Casey E. 2018. The effects of extrinsic factors on the structural and mechanical properties of Pseudomonas fluorescens biofilms: a combined study of nutrient concentrations and shear conditions. Colloids Surf B Biointerf. 165:127–134. doi:10.1016/j.colsurfb.2018.02.035
   PubMed Web of Science ®Google Scholar
• Anderson DC, Campbell EL, Meeks JC. 2006. A soluble 3D LC/MS/MS proteome of the filamentous cyanobacterium Nostoc punctiforme. J Proteome Res. 5:3096–3104. doi:10.1021/pr060272m
   PubMed Web of Science ®Google Scholar
• Baba M, Suzuki I, Shiraiwa Y. 2011. Proteomic analysis of high-CO(2)-inducible extracellular proteins in the unicellular green alga, Chlamydomonas reinhardtii. Plant Cell Physiol. 52:1302–1314. doi:10.1093/pcp/pcr078
   PubMed Web of Science ®Google Scholar
• Babele PK, Kumar J, Chaturvedi V. 2019. Proteomic de-regulation in cyanobacteria in response to abiotic stresses. Front Microbiol. 10:1–22. doi:10.3389/fmicb.2019.01315
   PubMed Web of Science ®Google Scholar
• Badger MR, Price GD. 2003. CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot. 54:609–622. doi:10.1093/jxb/erg076
   PubMed Web of Science ®Google Scholar
• Bakke R, Kommedal R, Kalvenes S. 2001. Quantification of biofilm accumulation by an optical approach. J Microbiol Methods. 44:13–26. doi:10.1016/S0167-7012(00)00236-0
   PubMed Web of Science ®Google Scholar
• Battchikova N, Muth-Pawlak D, Aro EM. 2018. Proteomics of cyanobacteria: current horizons. Curr Opin Biotechnol. 54:65–71. doi:10.1016/j.copbio.2018.02.012
   PubMed Web of Science ®Google Scholar
• Bharti A, Velmourougane K, Prasanna R. 2017. Phototrophic biofilms: diversity, ecology and applications. J Appl Phycol. 29:2729–2744. doi:10.1007/s10811-017-1172-9
   Web of Science ®Google Scholar
• Campos A, Danielsson G, Farinha AP, Kuruvilla J, Warholm P, Cristobal S. 2016. Shotgun proteomics to unravel marine mussel (Mytilus edulis) response to long-term exposure to low salinity and propranolol in a Baltic Sea microcosm. J Proteomics. 137:97–106. doi:10.1016/j.jprot.2016.01.010
   PubMed Web of Science ®Google Scholar
• Canny J. 1986. A computational approach to edge detection. IEEE Trans Pattern Anal Mach Intell. 8:679–698. doi: 10.1109/TPAMI.1986.4767851.
   PubMed Web of Science ®Google Scholar
• Carvalho C. 2018. Marine biofilms: a successful microbial strategy with economic implications. Front Mar Sci. 5:1–11. doi:10.3389/fmars.2018.00126
   PubMed Web of Science ®Google Scholar
• Chen M, Hernandez-Prieto MA, Loughlin PC, Li Y, Willows RD. 2019. Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions. BMC Genomics. 20:1–15. doi:10.1186/s12864-019-5587-3
   PubMed Web of Science ®Google Scholar
• Crawford RJ, Webb HK, Truong VK, Hasan J, Ivanova EP. 2012. Surface topographical factors influencing bacterial attachment. Adv Colloid Interface Sci. 179–182:142–149. doi:10.1016/j.cis.2012.06.015
   PubMed Web of Science ®Google Scholar
• Delauney L, Compère C, Lehaitre M. 2010. Biofouling protection for marine environmental sensors. Ocean Sci. 6:503–511. doi:10.5194/os-6-503-2010
   Web of Science ®Google Scholar
• Diaconu M, Kothe U, Schlünzen F, Fischer N, Harms JM, Tonevitsky AG, Stark H, Rodnina MV, Wahl MC. 2005. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTpase activation. Cell. 121:991–1004. doi:10.1016/j.cell.2005.04.015
   PubMed Web of Science ®Google Scholar
• Duda RO, Hart PE. 1972. Use of the Hough transformation to detect lines and curves in pictures. Commun Acm. 15:11–15. doi:10.1145/361237
   Web of Science ®Google Scholar
• Faria SI, Teixeira-Santos R, Romeu MJ, Morais J, Vasconcelos V, Mergulhão FJ. 2020. The relative importance of shear forces and surface hydrophobicity on biofilm formation by coccoid cyanobacteria. Polymers (Basel). 12:653. doi:10.3390/polym12030653
   Web of Science ®Google Scholar
• Favre L, Ortalo-Magné A, Pichereaux C, Gargaros A, Burlet-Schiltz O, Cotelle V, Culioli G. 2018. Metabolome and proteome changes between biofilm and planktonic phenotypes of the marine bacterium Pseudoalteromonas lipolytica TC8. Biofouling. 34:132–148. doi:10.1080/08927014.2017.1413551
   PubMed Web of Science ®Google Scholar
• Flemming H-C, Murthy PS, Venkatesan R, Cooksey K. 2009. Marine and industrial biofouling. Costerton JW, editor. Los Angeles: Springer Berlin Heidelberg.
   Google Scholar
• Heidari F, Hauer T, Zima J, Riahi H. 2018. New simple trichal cyanobacterial taxa isolated from radioactive thermal springs. Fottea. 18:137–149. doi:10.5507/fot.2017.024
   Web of Science ®Google Scholar
• Herschend J, Damholt ZBV, Marquard AM, Svensson B, Sørensen SJ, Hägglund P, Burmølle M. 2017. A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community. Sci Rep. 7:1–13. doi:10.1038/s41598-017-16633-6
   PubMed Web of Science ®Google Scholar
• Huang F, Parmryd I, Nilsson F, Persson AL, Pakrasi HB, Andersson B, Norling B. 2002. Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins. Mol Cell Proteom. 1:956–966. doi:10.1074/mcp.m200043-mcp200
   PubMed Web of Science ®Google Scholar
• Jahn M, Vialas V, Karlsen J, Maddalo G, Edfors F, Forsström B, Uhlén M, Käll L, Hudson EP. 2018. Growth of cyanobacteria is constrained by the abundance of light and carbon assimilation proteins. Cell Rep. 25:478–486.e8. doi:10.1016/j.celrep.2018.09.040
   PubMed Web of Science ®Google Scholar
• King RK, Flick GJ, Smith SA, Pierson MD, Boardman GD, Coale CW. 2006. Comparison of bacterial presence in biofilms on different materials commonly found in recirculating aquaculture systems. J Appl Aquac. 18:79–88. doi:10.1300/J028v18n01_05
   Google Scholar
• Kotai J. 1972. Instructions for the preparation of modified nutrient solution Z8 for algae. Blindern, Oslo: Norwegian Institute for Water Research; vol. 11, p. 5.
   Google Scholar
• Kurdrid P, Senachak J, Sirijuntarut M, Yutthanasirikul R, Phuengcharoen P, Jeamton W, Roytrakul S, Cheevadhanarak S, Hongsthong A. 2011. Comparative analysis of the Spirulina platensis subcellular proteome in response to low- and high-temperature stresses: uncovering cross-talk of signaling components. Proteome Sci. 9:39. doi:10.1186/1477-5956-9-39
   PubMed Web of Science ®Google Scholar
• Lau NS, Matsui M, Abdullah AA. 2015. Cyanobacteria: photoautotrophic microbial factories for the sustainable synthesis of industrial products. Biomed Res Int. 2015:754934. doi:10.1155/2015/754934
   PubMed Web of Science ®Google Scholar
• Leary DH, Li RW, Hamdan LJ, Hervey WJ, Lebedev N, Wang Z, Deschamps JR, Kusterbeck AW, Vora GJ. 2014. Integrated metagenomic and metaproteomic analyses of marine biofilm communities. Biofouling. 30:1211–1223. doi:10.1080/08927014.2014.977267
   PubMed Web of Science ®Google Scholar
• Liao Y, Williams TJ, Ye J, Charlesworth J, Burns BP, Poljak A, Raftery MJ, Cavicchioli R. 2016. Morphological and proteomic analysis of biofilms from the Antarctic archaeon. Sci Rep. 6:37454. doi:10.1038/srep3745
   PubMed Web of Science ®Google Scholar
• Lv J, Li N, Niu DK. 2008. Association between the availability of environmental resources and the atomic composition of organismal proteomes: evidence from Prochlorococcus strains living at different depths. Biochem Biophys Res Commun. 375:241–246. doi:10.1016/j.bbrc.2008.08.011
   PubMed Web of Science ®Google Scholar
• MacColl R. 1998. Cyanobacterial phycobilisomes. J Struct Biol. 124:311–334. doi:10.1006/jsbi.1998.4062
   PubMed Web of Science ®Google Scholar
• Manirafasha E, Ndikubwimana T, Zeng X, Lu Y, Jing K. 2016. Phycobiliprotein: potential microalgae derived pharmaceutical and biological reagent. Biochem Eng J. 109:282–296. doi:10.1016/j.bej.2016.01.025
   Web of Science ®Google Scholar
• Mayer MA, Borsdorf A, Wagner M, Hornegger J, Mardin CY, Tornow RP. 2012. Wavelet denoising of multiframe optical coherence tomography data. Biomed Opt Express. 3:572–589. doi:10.1364/BOE.3.000572
   PubMed Web of Science ®Google Scholar
• Mieszkin S, Callow ME, Callow JA. 2013. Interactions between microbial biofilms and marine fouling algae: a mini review. Biofouling. 29:1097–1113. doi:10.1080/08927014.2013.828712
   PubMed Web of Science ®Google Scholar
• Moreira JMR, Gomes LC, Simões M, Melo LF, Mergulhão FJ. 2015. The impact of material properties, nutrient load and shear stress on biofouling in food industries. Food Bioprod Process. 95:228–236. doi:10.1016/j.fbp.2015.05.011
   Web of Science ®Google Scholar
• Muthusamy S, Lundin D, Mamede Branca RM, Baltar F, González JM, Lehtiö J, Pinhassi J. 2017. Comparative proteomics reveals signature metabolisms of exponentially growing and stationary phase marine bacteria. Environ Microbiol. 19:2301–2319. doi:10.1111/1462-2920.13725
   PubMed Web of Science ®Google Scholar
• Nelson N, Yocum CF. 2006. Structure and function of photosystems I and II. Annu Rev Plant Biol. 57:521–565. doi:10.1146/annurev.arplant.57.032905.105350
   PubMed Web of Science ®Google Scholar
• Otsuka S, Suda S, Shibata S, Oyaizu H, Matsumoto S, Watanabe MM. 2001. A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the Bacteriological Code. Int J Syst Evol Microbiol. 51:873–879. doi:10.1099/00207713-51-3-873
   PubMed Web of Science ®Google Scholar
• Ow SY, Salim M, Noirel J, Evans C, Wright PC. 2011. Minimising iTRAQ ratio compression through understanding LC-MS elution dependence and high-resolution HILIC fractionation. Proteomics. 11:2341–2346. doi:10.1002/pmic.201000752
   PubMed Web of Science ®Google Scholar
• Pagels F, Guedes AC, Amaro HM, Kijjoa A, Vasconcelos V. 2019. Phycobiliproteins from cyanobacteria: chemistry and biotechnological applications. Biotechnol Adv. 37:422–443. doi:10.1016/j.biotechadv.2019.02.010
   PubMed Web of Science ®Google Scholar
• Pandhal J, Ow SY, Wright PC, Biggs CA. 2009. Comparative proteomics study of salt tolerance between a nonsequenced extremely halotolerant cyanobacterium and its mildly halotolerant relative using in vivo metabolic labeling and in vitro isobaric labeling. J Proteome Res. 8:818–828. doi:10.1021/pr800283q
   PubMed Web of Science ®Google Scholar
• Parnasa R, Nagar E, Sendersky E, Reich Z, Simkovsky R, Golden S, Schwarz R. 2016. Small secreted proteins enable biofilm development in the cyanobacterium Synechococcus elongatus. Sci Rep. 6:32209. doi:10.1038/srep32209
   PubMed Web of Science ®Google Scholar
• Perkerson Iii RB, Johansen JR, Kováčik L, Brand J, Kaštovský J, Casamatta DA. 2011. A unique pseudanabaenalean (Cyanobacteria) genus Nodosilinea gen. nov. based on morphological and molecular DATA(1). J Phycol. 47:1397–1412. doi:10.1111/j.1529-8817.2011.01077.x
   PubMed Web of Science ®Google Scholar
• Pisareva T, Shumskaya M, Maddalo G, Ilag L, Norling B. 2007. Proteomics of Synechocystis sp. PCC 6803. Identification of novel integral plasma membrane proteins. Febs J. 274:791–804. doi:10.1111/j.1742-4658.2006.05624.x
   PubMed Web of Science ®Google Scholar
• Porra R, Thompson W, Kriedemann P. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta. 975:384–394. doi:10.1016/S0005-2728(89)80347-0
   Web of Science ®Google Scholar
• Qayyum S, Sharma D, Bisht D, Khan AU. 2016. Protein translation machinery holds a key for transition of planktonic cells to biofilm state in Enterococcus faecalis: a proteomic approach. Biochem Biophys Res Commun. 474:652–659. doi:10.1016/j.bbrc.2016.04.145
   PubMed Web of Science ®Google Scholar
• Radzi R, Muangmai N, Broady P, Wan Omar WM, Lavoue S, Convey P, Merican F. 2019. Nodosilinea signiensis sp. nov. (Leptolyngbyaceae, Synechococcales), a new terrestrial cyanobacterium isolated from mats collected on Signy Island, South Orkney Islands, Antarctica. PLoS One. 14:e0224395. doi:10.1371/journal.pone.0224395
   PubMed Web of Science ®Google Scholar
• Ramos V, Morais J, Castelo-Branco R, Pinheiro Â, Martins J, Regueiras A, Pereira AL, Lopes VR, Frazão B, Gomes D, et al. 2018. Cyanobacterial diversity held in microbial biological resource centers as a biotechnological asset: the case study of the newly established LEGE culture collection. J Appl Phycol. 30:1437–1451. doi:10.1007/s10811-017-1369-y
   PubMed Web of Science ®Google Scholar
• Romeu MJ, Alves P, Morais J, Miranda JM, de Jong ED, Sjollema J, Ramos V, Vasconcelos V, Mergulhão F. 2019. Biofilm formation behaviour of marine filamentous cyanobacterial strains in controlled hydrodynamic conditions. Environ Microbiol. 21:4411–4424. doi:10.1111/1462-2920.14807
   PubMed Web of Science ®Google Scholar
• Slabas AR, Suzuki I, Murata N, Simon WJ, Hall JJ. 2006. Proteomic analysis of the heat shock response in Synechocystis PCC6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics. 6:845–864. doi:10.1002/pmic.200500196
   PubMed Web of Science ®Google Scholar
• Sonani RR, Gupta GD, Madamwar D, Kumar V. 2015. Crystal structure of allophycocyanin from marine cyanobacterium Phormidium sp. Plos One. 10:e0124580. doi:10.1371/journal.pone.0124580
   PubMed Web of Science ®Google Scholar
• Sun T, Li S, Song X, Diao J, Chen L, Zhang W. 2018. Toolboxes for cyanobacteria: recent advances and future direction. Biotechnol Adv. 36:1293–1307. doi:10.1016/j.biotechadv.2018.04.007
   PubMed Web of Science ®Google Scholar
• Taylor DA. 1996. Introduction to marine engineering. Burlington, MA: Butterworth-Heinemann.
   Google Scholar
• Telegdi J, Trif L, Románszki L. 2016. Smart anti-biofouling composite coatings for naval applications. In: Montemor MF, editor. Smart composite coatings and membranes transport, structural, environmental and energy applications. Cambridge, UK: Woodhead Publishing; p. 123–155.
   Google Scholar
• Teodósio JS, Simões M, Melo LF, Mergulhão FJ. 2011. Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling. 27:1–11. doi:10.1080/08927014.2010.535206
   PubMed Web of Science ®Google Scholar
• Vázquez-Martínez J, Gutierrez-Villagomez JM, Fonseca-García C, Ramírez-Chávez E, Mondragón-Sánchez ML, Partida-Martínez L, Johansen JR, Molina-Torres J. 2018. Nodosilinea chupicuarensis sp. nov. (Leptolyngbyaceae, Synechococcales) a subaerial cyanobacterium isolated from a stone monument in central Mexico. Phytotaxa. 334:167. doi:10.11646/phytotaxa.334.2.6
   Web of Science ®Google Scholar
• Wang N, Sadiq FA, Li S, He G, Yuan L. 2020. Tandem mass tag-based quantitative proteomics reveals the regulators in biofilm formation and biofilm control of Bacillus licheniformis. Food Control. 110:107029. doi:10.1016/j.foodcont.2019.107029
   Web of Science ®Google Scholar
• Wang Y, Stessman DJ, Spalding MH. 2015. The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: how Chlamydomonas works against the gradient. Plant J. 82:429–448. doi:10.1111/tpj.12829
   PubMed Web of Science ®Google Scholar
• Wiśniewski JR, Zougman A, Nagaraj N, Mann M. 2009. Universal sample preparation method for proteome analysis. Nat Methods. 6:359–362. doi:10.1038/nmeth.1322
   PubMed Web of Science ®Google Scholar
• Wood ZA, Schröder E, Harris JR, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci. 28:32–40. doi:10.1016/S0968-0004(02)00003-8
   PubMed Web of Science ®Google Scholar