Skip to main content
SpringerLink
Log in

The importance of being fast: comparative kinetics of vertical migration and non-photochemical quenching of benthic diatoms under light stress

Marine Biology Aims and scope Submit manuscript

Cite this article

Abstract

Sediment-inhabiting microphytobenthos (MPB) is dominated by raphid pennate diatoms that use vertical migration (VM) and the xanthophyll cycle (XC) as main photoprotective mechanisms against excess light. This study compares the short-term kinetics of activation of the two processes upon exposure to high light. The light response of VM was studied with temporal resolution of minutes, by using a new experimental approach (a ‘multi-actinic imaging’ system) based on the combination of (1) simultaneous application of multiple levels of incident light (50–1350 µmol m−2 s−1) to replicated samples, through the projection of spatially separated beams of actinic light, and (2) reflectance-based imaging of MPB surface biomass, using a modified chlorophyll fluorescence imaging system with red and infrared bandpass filters. The induction kinetics of the XC was inferred by measuring the activation of non-photochemical quenching (NPQ) of chlorophyll fluorescence, upon exposure to high light, on MPB suspensions. The possibility to trace VM with high temporal resolution allowed to find that the migratory photoresponse is much faster than previously reported, occurring at the scale of a few minutes. Surface biomass decreased by more than 30 % of total induced change during the first 2.5 min of light exposure and reached a steady state after 15 min. More importantly, it was found that the light induction of VM and NPQ largely overlaps in time, suggesting a complex interdependency in the regulation of the two mechanisms. These results further indicate that VM is fast enough to modulate the light regime experienced by the cells and to affect this photoacclimation state and their photoprotective capacity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Admiraal W (1984) The ecology of estuarine sediment-inhabiting diatoms. Prog Phycol Res 3:269–322

    Google Scholar 

  • Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192. doi:10.1038/nature08057

    Article  CAS  Google Scholar 

  • Arsalane W, Rousseau B, Duval JC (1994) Influence of the pool size of the xanthophyll cycle on the effects of light stress in a diatom: competition between photoprotection and photoinhibition. Photochem Photobiol 60:237–243. doi:10.1111/j.1751-1097.1994.tb05097.x

    Article  CAS  Google Scholar 

  • Barnett A, Méléder V, Blommaert L, Lepetit B, Gaudin P, Vyverman W, Sabbe K, Dupuy C, Lavaud J (2015) Growth form defines physiological photoprotective capacity in intertidal benthic diatoms. ISME J 9:32–45. doi:10.1038/ismej.2014.105

    Article  CAS  Google Scholar 

  • Cartaxana P, Serôdio J (2008) Inhibiting diatom motility: a new tool for the study of the photophysiology of intertidal microphytobenthic biofilms. Limnol Oceanogr Methods 6:466–476. doi:10.4319/lom.2008.6.466

    Article  CAS  Google Scholar 

  • Cartaxana P, Ruivo M, Hubas C, Davidson I, Serôdio J, Jesus B (2011) Physiological versus behavioral photoprotection in intertidal epipelic and epipsammic benthic diatom communities. J Exp Mar Biol Ecol 405:120–127. doi:10.1016/j.jembe.2011.05.027

    Article  Google Scholar 

  • Cohn SA, Bahena M, Davis JT, Ragland RL, Rauschenberg CD, Smith BJ (2004) Characterisation of the diatom photophobic response to high irradiance. Diatom Res 19:167–179. doi:10.1080/0269249X.2004.9705869

    Article  Google Scholar 

  • Cohn SA, Halpin D, Hawley N, Ismail A, Kaplan Z, Kordes T, Kuhn J, Macke W, Marhaver K, Ness B, Olszewski S, Pike A, Rice E, Sbarboro J, Wolske A, Zapata Y (2015) Comparative analysis of light-stimulated motility responses in three diatom species. Diatom Res 30:1–13. doi:10.1080/0269249X.2015.1058295

    Article  Google Scholar 

  • Consalvey M, Paterson DM, Underwood GJC (2004) The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res 19:181–202

    Article  Google Scholar 

  • Cruz S, Serôdio J (2008) Relationship of rapid light curves of variable fluorescence to photoacclimation and non-photochemical quenching in a benthic diatom. Aquat Bot 88:256–264. doi:10.1016/j.aquabot.2007.11.001

    Article  CAS  Google Scholar 

  • D’Haese D, Vandermeiren K, Caubergs RJ, Guisez Y, De Temmerman L, Horemans N (2004) Non-photochemical quenching kinetics during the dark to light transition in relation to the formation of antheraxanthin and zeaxanthin. J Theor Biol 227:175–186. doi:10.1016/j.jtbi.2003.10.011

    Article  Google Scholar 

  • Du GY, Oak J-H, Li H, Chung I-K (2010) Effect of light and sediment grain size on the vertical migration of benthic diatoms. Algae 25:133–140. doi:10.4490/algae.2010.25.3.133

    Article  Google Scholar 

  • Du GY, Li WT, Li H, Chung IK (2012) Migratory responses of benthic diatoms to light and temperature monitored by chlorophyll fluorescence. J Plant Biol 55:159–164. doi:10.1007/s12374-011-9200-9

    Article  CAS  Google Scholar 

  • Eaton JW, Moss B (1966) The estimation of numbers and pigment content in epipelic algal populations. Limnol Oceanogr 11:584–595. doi:10.4319/lo.1966.11.4.0584

    Article  Google Scholar 

  • Edgar L, Pickett-Heaps J (1984) Diatom locomotion. Prog Phycol Res 3:47–88

    Article  Google Scholar 

  • Ezequiel J, Laviale M, Frankenbach S, Cartaxana P, Serôdio J (2015) Photoacclimation state determines the photobehaviour of motile microalgae: the case of a benthic diatom. J Exp Mar Biol Ecol 468:11–20. doi:10.1016/j.jembe.2015.03.004

    Article  Google Scholar 

  • Forster RM, Kromkamp JC (2004) Modelling the effects of chlorophyll fluorescence from subsurface layers on photosynthetic efficiency measurements in microphytobenthic algae. Mar Ecol Prog Ser 284:9–22. doi:10.3354/meps284009

    Article  Google Scholar 

  • Frankenbach S, Pais C, Martinez M, Laviale M, Ezequiel J, Serôdio J (2014) Evidence for gravitactic behaviour in benthic diatoms. Eur J Phycol 49:429–435. doi:10.1080/09670262.2014.974218

    Article  Google Scholar 

  • Furukawa T, Watanabe M, Shihira-Ishikawa I (1998) Green- and blue-light-mediated chloroplast migration in the centric diatom Pleurosira laevis. Protoplasma 203:214–220. doi:10.1007/BF01279479

    Article  Google Scholar 

  • Harper MA (1977) Movements. In: Werner D (ed) The Biology of diatoms. Blackwell, Oxford, pp 224–249

    Google Scholar 

  • Hopkins JT (1963) A study of the diatoms of the Ouse Estuary, Sussex. I. The movement of the mudflat diatoms in response to some chemical and physical changes. J Mar Biol Assoc UK 43:653–663. doi:10.1017/S0025315400025595

    Article  Google Scholar 

  • Jesus B, Mendes CR, Brotas V, Paterson DM (2006a) Effect of sediment type on microphytobenthos vertical distribution: modelling the productive biomass and improving ground truth measurements. J Exp Mar Biol Ecol 332:60–74. doi:10.1016/j.jembe.2005.11.005

    Article  Google Scholar 

  • Jesus B, Perkins RG, Consalvey M, Brotas V, Paterson DM (2006b) Effects of vertical migrations by benthic microalgae on fluorescence measurements of photophysiology. Mar Ecol Prog Ser 315:55–66. doi:10.3354/meps315055

    Article  CAS  Google Scholar 

  • Jesus B, Mouget J, Perkins RG (2008) Detection of diatom xanthophyll cycle using spectral reflectance. J Phycol 44:1349–1359. doi:10.1111/j.1529-8817.2008.00583.x

    Article  CAS  Google Scholar 

  • Jesus B, Brotas V, Ribeiro L, Mendes R, Cartaxana P, Paterson M (2009) Adaptations of microphytobenthos assemblages to sediment type and tidal position. Cont Shelf Res 29:1624–1634. doi:10.1016/j.csr.2009.05.006

    Article  Google Scholar 

  • Juneau P, Barnett A, Méléder V, Dupuy C, Lavaud J (2015) Combined effect of high light and high salinity on the regulation of photosynthesis in three diatom species belonging to the main growth forms of intertidal flat inhabiting microphytobenthos. J Exp Mar Biol Ecol 463:95–104. doi:10.1016/j.jembe.2014.11.003

    Article  CAS  Google Scholar 

  • Kato MC, Hikosaka K, Hirotsu N, Makino A, Hirose T (2003) The excess light energy that is neither utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant Cell Physiol 44:318–325. doi:10.1093/pcp/pcg045

    Article  CAS  Google Scholar 

  • Kelly JA, Honeywill C, Paterson DM (2001) Microscale analysis of chlorophyll-a in cohesive, intertidal sediments: the implications of microphytobenthos distribution. J Mar Biol Assoc UK 81:151–162. doi:10.1017/S0025315401003496

    Article  CAS  Google Scholar 

  • Kingston MB (1999) Effect of light on vertical migration and photosynthesis of Euglena proxima (Euglenophyta). J Phycol 35:245–253. doi:10.1046/j.1529-8817.1999.3520245.x

    Article  Google Scholar 

  • Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665. doi:10.4319/lo.1993.38.8.1646

    Article  CAS  Google Scholar 

  • Koller D (1990) Light-driven leaf movements. Plant, Cell Environ 13:615–632. doi:10.1111/j.1365-3040.1990.tb01079.x

    Article  Google Scholar 

  • Kooistra H, Gersonde R, Medlin L, Mann D (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski PG, Knoll A (eds) Evolution of Primary Producers in the Sea. Elsevier Academic Press, Amsterdam, pp 207–249

    Chapter  Google Scholar 

  • Kornyeyev D, Logan BA, Holaday AS (2010) Excitation pressure as a measure of the sensitivity of photosystem II to photoinactivation. Funct Plant Biol 37:943–951. doi:10.1071/FP09276

    Article  CAS  Google Scholar 

  • Kromkamp J, Barranguet C, Peene J (1998) Determination of microphytobenthos PSII quantum yield efficiency and photosynthetic activity by means of variable chlorophyll fluorescence. Mar Ecol Prog Ser 162:45–55. doi:10.3354/meps162045

    Article  CAS  Google Scholar 

  • Latowski D, Burda K, Strzałka K (2000) A mathematical model describing kinetics of conversion of violaxanthin to zeaxanthin via intermediate antheraxanthin by the xanthophyll cycle enzyme violaxanthin de-epoxidase. J Theor Biol 206:507–514. doi:10.1006/jtbi.2000.2141

    Article  CAS  Google Scholar 

  • Lavaud J, Goss R (2014) The peculiar features of non-photochemical fluorescence quenching in diatoms and brown algae. In: Adams B, Garab G, Adams W, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht, pp 421–443

    Google Scholar 

  • Lavaud J, Rousseau B, Etienne AL (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137. doi:10.1046/j.1529-8817.2004.03026.x

    Article  Google Scholar 

  • Lavaud J, Strzepek RF, Kroth PG (2007) Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52:1188–1194. doi:10.4319/lo.2007.52.3.1188

    Article  CAS  Google Scholar 

  • Laviale M, Barnett A, Ezequiel J, Lepetit B, Frankenbach S, Méléder V, Serôdio J, Lavaud J (2015) Response of intertidal benthic microalgal biofilms to a coupled light-temperature stress: evidence for latitudinal adaptation along the Atlantic coast of Southern Europe. Environ Microbiol 17:3662–3677. doi:10.1111/1462-2920.12728

    Article  CAS  Google Scholar 

  • Leal MC, Jesus B, Ezequiel J, Calado R, Rocha RJM, Cartaxana P, Serôdio J (2014) Concurrent imaging of chlorophyll fluorescence, chlorophyll a content and green fluorescent proteins-like proteins of symbiotic cnidarians. Mar Ecol. doi:10.1111/maec.12164.10.1111/maec.12164

    Google Scholar 

  • MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19:186–201. doi:10.2307/1352224

    Article  Google Scholar 

  • Mclachlan DH, Brownlee C, Taylor AR, Geider RJ, Underwood GJC (2009) Light-induced motile responses of the estuarine benthic diatoms Navicula perminuta and Cylindrotheca closterium (Bacillariophyceae). J Phycol 45:592–599. doi:10.1111/j.1529-8817.2009.00681.x

    Article  Google Scholar 

  • Mouget J, Perkins R, Consalvey M, Lefebvre S (2008) Migration or photoacclimation to prevent high irradiance and UV-B damage in marine microphytobenthic communities. Aquat Microb Ecol 52:223–232. doi:10.3354/ame01218

    Article  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566. doi:10.1104/pp.125.4.1558

    Article  Google Scholar 

  • Olaizola M, Yamamoto HY (1994) Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). J Phycol 30:606–612. doi:10.1111/1529-8817.ep11471363

    Article  CAS  Google Scholar 

  • Öquist G (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186:450–460. doi:10.1007/BF00195327

    Article  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparison of shade and sun plants. In: Baker N, Bowyer J (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Bios Scientific, Oxford, pp 1–24

    Google Scholar 

  • Park Y-I, Chow WS, Anderson JM (1995) The quantum yield of photoinactivation of photosystem II in pea leaves is greater at low than high photon exposure. Plant Cell Physiol 36:1163–1167

    CAS  Google Scholar 

  • Park Y-I, Chow WS, Anderson JM (1996a) Chloroplast movement in the shade plant Tradescanfia albiflora helps protect photosystem II against light stress. Plant Physiol 111:867–875. doi:10.1104/pp.111.3.867

    CAS  Google Scholar 

  • Park Y-I, Chow WS, Anderson JM, Hurry VM, Hurryb VM (1996b) Differential susceptibility of photosystem II to light stress in light acclimated pea leaves depends on the capacity for photochemical and non-radiative dissipation of light. Plant Sci 115:137–149. doi:10.1016/0168-9452(96)04339-7

    Article  CAS  Google Scholar 

  • Paterson DM, Wiltshire KH, Miles A, Blackburn J, Davidson I, Yates MG, Mcgrorty S, Eastwood JA (1998) Microbiological mediation of spectral reflectance from intertidal cohesive sediments. Limnol Oceanogr 43:1207–1221

    Article  Google Scholar 

  • Perkins RG, Underwood GJC, Brotas V, Snow GC, Jesus B, Ribeiro L (2001) Responses of microphytobenthos to light: primary production and carbohydrate allocation over an emersion period. Mar Ecol Prog Ser 223:101–112. doi:10.3354/meps223101

    Article  Google Scholar 

  • Perkins RG, Mouget JL, Lefebvre S, Lavaud J (2006) Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic diatoms. Mar Biol 149:703–712

    Article  Google Scholar 

  • Perkins R, Lavaud J, Serôdio J, Mouget J, Cartaxana P, Rosa P, Barille L, Brotas V, Jesus B (2010) Vertical cell movement is a primary response of intertidal benthic biofilms to increasing light dose. Mar Ecol Prog Ser 416:93–103. doi:10.3354/meps08787

    Article  CAS  Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237. doi:10.1016/j.aquabot.2005.02.006

    Article  CAS  Google Scholar 

  • Ribeiro L, Brotas V, Rincé Y, Jesus B (2013) Structure and diversity of intertidal benthic diatom assemblages in contrasting shores: a case study from the Tagus Estuary. J Phycol 49:258–270. doi:10.1111/jpy.12031

    Article  Google Scholar 

  • Rouse J, Haas R, Schell J, Deering D (1973) Monitoring vegetation systems in the great plains with ERTS. Third Earth Resources Technology Satellite Symposium, NASA SP-351. NASA, Washington, D.C., pp 309–317

  • Schreiber U, Klughammer C, Kolbowski J (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynth Res 113:127–144. doi:10.1007/s11120-012-9758-1

    Article  CAS  Google Scholar 

  • Serôdio J (2004) Analysis of variable chlorophyll fluorescence in microphytobenthos assemblages: implications of the use of depth-integrated measurements. Aquat Microb Ecol 36:137–152. doi:10.3354/ame036137

    Article  Google Scholar 

  • Serôdio J, Lavaud J (2011) A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res 108:61–76. doi:10.1007/s11120-011-9654-0

    Article  Google Scholar 

  • Serôdio J, Marques da Silva J, Catarino F (2001) Use of in vivo chlorophyll a fluorescence to quantify short-term variations in the productive biomass of intertidal microphytobenthos. Mar Ecol Prog Ser 218:45–61. doi:10.3354/meps218045

    Article  Google Scholar 

  • Serôdio J, Cruz S, Vieira S, Brotas V (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. J Exp Mar Biol Ecol 326:157–169. doi:10.1016/j.jembe.2005.05.011

    Article  Google Scholar 

  • Serôdio J, Coelho H, Vieira S, Cruz S (2006) Microphytobenthos vertical migratory photoresponse as characterised by light-response curves of surface biomass. Estuar Coast Shelf Sci 68:547–556. doi:10.1016/j.ecss.2006.03.005

    Article  Google Scholar 

  • Serôdio J, Cartaxana P, Coelho H, Vieira S (2009) Effects of chlorophyll fluorescence on the estimation of microphytobenthos biomass using spectral reflectance indices. Remote Sens Environ 113:1760–1768. doi:10.1016/j.rse.2009.04.003

    Article  Google Scholar 

  • Serôdio J, Ezequiel J, Barnett A, Mouget J, Méléder V, Laviale M, Lavaud J (2012) Efficiency of photoprotection in microphytobenthos: role of vertical migration and the xanthophyll cycle against photoinhibition. Aquat Microb Ecol 67:161–175. doi:10.3354/ame01591

    Article  Google Scholar 

  • Serôdio J, Ezequiel J, Frommlet J, Laviale M, Lavaud J (2013) A method for the rapid generation of nonsequential light-response curves of chlorophyll fluorescence. Plant Physiol 163:1089–1102. doi:10.1104/pp.113.225243

    Article  Google Scholar 

  • Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303. doi:10.1016/B978-0-12-405210-9.00007-2

    Article  Google Scholar 

  • Underwood GJC, Kromkamp J (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Adv Ecol Res 29:93–153

    Article  CAS  Google Scholar 

  • Underwood GJC, Nilsson C, Sundback K, Wulff A (1999) Short-Term effects of UVB radiation on chlorophyll fluorescence, biomass, pigments, and carbohydrate fractions in a benthic diatom mat. J Phycol 35:656–666. doi:10.1046/j.1529-8817.1999.3540656.x

    Article  CAS  Google Scholar 

  • Van Leeuwe MA, Brotas V, Consalvey M, Forster RM, Gillespie D, Jesus B, Roggeveld J, Gieskes WWC (2008) Photoacclimation in microphytobenthos and the role of xanthophyll pigments. Eur J Phycol 43:123–132. doi:10.1080/01431160110106096

    Article  Google Scholar 

  • Wada M (2013) Chloroplast movement. Plant Sci 210:177–182. doi:10.1016/j.plantsci.2013.05.016

    Article  CAS  Google Scholar 

  • Waring J, Baker NR, Underwood GJC (2007) Responses of estuarine intertidal microphytobenthic algal assemblages to enhanced ultraviolet B radiation. Glob Change Biol 13:1398–1413. doi:10.1111/j.1365-2486.2007.01378.x

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the Fundação para a Ciência e a Tecnologia (FCT) through project MigROS (PTDC/MAR/112473/2009; ML postdoc fellowship), co-funded by COMPETE/QREN/UE, and doctoral Grant SFRH/BD/86788/2012 (SF). The authors would like to thank Sandra C. Craveiro for help in diatom species identification and to two anonymous reviewers for their critical comments on the manuscript.

Author information

Authors and Affiliations

  1. Departamento de Biologia and CESAM – Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193, Aveiro, Portugal

    Martin Laviale, Silja Frankenbach & João Serôdio

  2. UPMC Univ Paris 06, CNRS, INRIA, Laboratoire d’Océanographie de Villefranche-sur-Mer (LOV), Sorbonne Universités, 181 chemin du Lazaret, 06230, Villefranche-Sur-Mer, France

    Martin Laviale

Authors
  1. Martin Laviale
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Silja Frankenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. João Serôdio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to João Serôdio.

Additional information

Responsible Editor: K. Bischof.

Reviewed by D. Campbell, J. Kromkamp.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Laviale, M., Frankenbach, S. & Serôdio, J. The importance of being fast: comparative kinetics of vertical migration and non-photochemical quenching of benthic diatoms under light stress. Mar Biol 163, 10 (2016). https://doi.org/10.1007/s00227-015-2793-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-015-2793-7

Keywords

search

Navigation