Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-20T00:21:26.978Z Has data issue: false hasContentIssue false

Combined effects of high temperature and light on the photosynthetic parameters and recovery of temperate microphytobenthos in Browns River, Tasmania

Published online by Cambridge University Press:  21 September 2022

Sazlina Salleh*
Affiliation:
Centre for Policy Research and International Studies (CenPRIS), Universiti Sains Malaysia, 11800, Minden, Pulau Pinang, Malaysia Center for Marine and Coastal Studies (CEMACS), Universiti Sains Malaysia, 11800, Minden, Pulau Pinang, Malaysia
Andrew McMinn
Affiliation:
Institute of Marine and Antarctic Studies (IMAS), University of Tasmania, Box 252-77, Hobart 7001, Tasmania, Australia College of Life Sciences, Ocean University of China, Qingdao, China
*
Author for correspondence: Sazlina Salleh, E-mail: [email protected]

Abstract

Microphytobenthos (MPB) communities are responsible for most primary production in shallow intertidal mudflats. The effects of short-term changes in temperature and light (1200, 500 and 0 μmol photons m−2 s−1) on the photosynthetic activity of intertidal MPB communities of Browns River, Tasmania, during winter (0, 5, 10 and 15°C) and summer (20, 25, 30, 35 and 40°C) were examined using a Pulse Amplitude Modulated (Water PAM) fluorometer. The MPB communities were primarily dominated by the diatom genera Navicula, Cocconeis and Amphora, with a difference in species dominance during seasons. During summer, Amphora coffeaeformis dominated communities were significantly impacted by temperatures above 30°C regardless of light intensities. The MPB was able to photosynthesize at temperatures only up to 25°C. The rETRmax at 25°C, ranged from 39.18 ± 3.42 (500 μmol photons m−2 s−1) to 22.83 ± 1.05 (0 μmol photons m−2 s−1), which was lower than the values recorded at an equivalent irradiance in in-situ summer. However, if ambient temperature exceeds 25°C in summer, it is likely that the photosynthetic capabilities of the MPB will be diminished and it will cause irreversible photoinhibition.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

An, SM, Choi, DH and Noh, JH (2020) High-throughput sequencing analysis reveals dynamic seasonal succession of diatom assemblages in a temperate tidal flat. Estuarine, Coastal and Shelf Science 237, 106686.CrossRefGoogle Scholar
Anning, T, Harris, G and Geider, RJ (2001) Thermal acclimation in the marine diatom Chaetoceros calcitrans (Bacillariophyceae). European Journal of Phycology 36, 233241.CrossRefGoogle Scholar
Béchet, Q, Laviale, M, Arsapin, N, Bonnefond, H and Bernard, O (2017) Modeling the impact of high temperatures on microalgal viability and photosynthetic activity. Biotechnology for Biofuels 10, 136.Google ScholarPubMed
Blanchard, GF, Guarini, JM, Gros, P and Richard, P (1997) Seasonal effect on the relationship between the photosynthetic capacity of intertidal microphytobenthos and temperature. Journal of Phycology 33, 723728.CrossRefGoogle Scholar
Blommaert, L, Huysman, MJ, Vyverman, W, Lavaud, J and Sabbe, K (2017) Contrasting NPQ dynamics and xanthophyll cycling in a motile and a non-motile intertidal benthic diatom. Limnology and Oceanography 62, 14661479.CrossRefGoogle Scholar
Blommaert, L, Lavaud, J, Vyverman, W and Sabbe, K (2018) Behavioural vs physiological photoprotection in epipelic and epipsammic benthic diatoms. European Journal of Phycology 53, 149155.CrossRefGoogle Scholar
Cartaxana, P, Domingues, N, Cruz, S, Jesus, B, Laviale, M, Serôdio, J and da Silva, JM (2013) Photoinhibition in benthic diatom assemblages under light stress. Aquatic Microbial Ecolology 70, 8792.CrossRefGoogle Scholar
Casper-Lindley, C and Björkman, O (1998) Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynthesis Research 56, 277289.CrossRefGoogle Scholar
Castrejon, ES (1999) Structure of benthic diatom assemblages from a mangrove environment in a Mexican subtropical lagoon. Biotropica 31, 4870.Google Scholar
Claquin, P, Probert, I, Lefebvre, S and Veron, B (2008) Effects of temperature on photosynthetic parameters and TEP production in eight species of marine diatom. Aquatic Microbial Ecology 51, 111.CrossRefGoogle Scholar
Coles, JF and Jones, RC (2000) Effect of temperature on photosynthesis-light response and growth of four phytoplankton species isolated from a tidal freshwater river. Journal of Phycology 36, 716.CrossRefGoogle Scholar
Consalvey, M, Jesus, B, Perkins, RG, Brotas, V, Underwood, GJC and Paterson, DM (2004 a) Monitoring migration and measuring biomass in benthic biofilms: the effects of dark/far-red adaptation and vertical migration on fluorescence measurements. Photosynthesis Research 81, 91101.CrossRefGoogle ScholarPubMed
Consalvey, M, Paterson, DM and Underwood, GJC (2004 b) The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Research 19, 181202.CrossRefGoogle Scholar
Consalvey, M, Perkins, RG, Paterson, DM and Underwood, GJC (2005) PAM fluorescence: a beginners guide for benthic diatomists. Diatom Research 20, 122.CrossRefGoogle Scholar
Cook, SS, Roberts, JL, Hallegraeff, GM and McMinn, A (2007) Impact of canal development on intertidal microalgal productivity: comparative assessment of Patterson Lakes and Ralphs Bay, South East Australia. Journal of Coastal Conservation 11, 171181.CrossRefGoogle Scholar
Cooper, SR (1995) Diatoms in sediment cores from the mesohaline Chesapeake Bay, USA. Diatom Research 10, 3989.CrossRefGoogle Scholar
Davison, IR (1991) Environmental effects on algal photosynthesis: temperature. Journal of Phycology 27, 28.CrossRefGoogle Scholar
Du, G, Yan, H, Liu, C and Mao, Y (2018) Behavioral and physiological photoresponses to light intensity by intertidal microphytobenthos. Journal of Oceanology and Limnology 36, 293304.CrossRefGoogle Scholar
El-Sabaawi, R and Harrison, PJ (2006) Interactive effects of irradiance and temperature on the photosynthetic physiology of the pennate diatom Pseudo-nitzschia granii (Baciliariophyceae) from the Northeast Subarctic Pacific. Journal of Phycology 42, 778785.CrossRefGoogle Scholar
Falkowski, PG and Raven, JA (1997) Aquatic Photosynthesis. Boston, MA: Blackwell Science, p. 375.Google Scholar
Falkowski, PG and Raven, JA (2007) Aquatic Photosynthesis, 1st ed. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Genty, B, Briantais, JM and Baker N, R (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimia et Biophysica Acta 990, 8792.CrossRefGoogle Scholar
Gleich, SJ, Plough, LV and Glibert, PM (2020) Photosynthetic efficiency and nutrient physiology of the diatom Thalassiosira pseudonana at three growth temperatures. Marine Biology 167, 113.CrossRefGoogle Scholar
González-Guerrero, LA, Vásquez-Elizondo, RM, López-Londoño, T, Hernán, G, Iglesias-Prieto, R and Enríquez, S (2022) Validation of parameters and protocols derived from chlorophyll a fluorescence commonly utilised in marine ecophysiological studies. Functional Plant Biology 49, 517532.CrossRefGoogle ScholarPubMed
Goss, R and Lepetit, B (2015) Biodiversity of NPQ. Journal of Plant Physiology 172, 1332.CrossRefGoogle ScholarPubMed
Hancke, K and Glud, RN (2004) Temperature effects on respiration and photosynthesis in three diatom-dominated benthic communities. Aquatic Microbial Ecology 37, 265281.CrossRefGoogle Scholar
Holm-Hansen, O, Lorenzen, CJ, Holmes, RW and Strickland, JDH (1965) Fluorometric determination of chlorophyll. Journal du Conseil 30, 315.CrossRefGoogle Scholar
Ibelings, BW (1996) Changes in photosynthesis in response to combined irradiance and temperature stress in cyanobacterial surface waterblooms. Journal of Phycology 32, 549557.CrossRefGoogle Scholar
IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. New York, NY: Cambridge University Press, 127.Google Scholar
Jassby, AD and Platt, T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography 21, 540547.CrossRefGoogle Scholar
Jordan, L, McMinn, A and Thompson, P (2010) Diurnal changes of photoadaptive pigments in microphytobenthos. Journal of the Marine Biological Association of the United Kingdom 90, 10251032.CrossRefGoogle Scholar
Jordan, L, McMinn, A and Wotherspoon, S (2008) Diurnal and monthly vertical profiles of benthic diatom within intertidal sediments from two temperate localities. Marine and Freshwater Research 59, 931939.CrossRefGoogle Scholar
Kirk, JTO (1994) Light and Photosynthesis in Aquatic Ecosystems. Cambridge: Cambridge University Press, 509 pp.CrossRefGoogle Scholar
Lambrev, PH, Miloslavina, Y, Jahns, P and Holzwarth, AR (2012) On the relationship between non-photochemical quenching and photoprotection of photosystem II. Biochimica et Biophysica Acta 1817, 760769.CrossRefGoogle ScholarPubMed
Lavaud, J and Goss, R (2014) The peculiar features of non-photochemical fluorescence quenching in diatoms and brown algae. In Demmig-Adams, B, Garab, G, Adams III, W and Govindjee, (eds), Non-photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Dordrecht: Springer, pp. 421443.CrossRefGoogle Scholar
Laviale, M, Barnett, A, Ezequiel, J, Lepetit, B, Frankenbach, S, Méléder, V, Serôdio, J and 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. Environmental Microbiology 17, 36623677.Google ScholarPubMed
Laviale, M, Frankenbach, S and Serôdio, J (2016) The importance of being fast: comparative kinetics of vertical migration and non-photochemical quenching of benthic diatoms under light stress. Marine Biology 163, 10.CrossRefGoogle Scholar
Lee, SH and McMinn, A (2013) Physiological response of temperate microphytobenthos to freezing temperatures. Journal of the Marine Biological Association of the United Kingdom 93, 20392047.CrossRefGoogle Scholar
Maxwell, K and Johnson, GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659668.CrossRefGoogle ScholarPubMed
McMinn, A and Hattori, H (2006) Effect of time of day on the recovery from light exposure in ice algae from Saroma Ko lagoon, Hokkaido. Polar Bioscience 20, 3036.Google Scholar
Migné, A, Spilmont, N and Davoult, D (2004) In situ measurements of benthic primary production during emersion: seasonal variations and annual production in the Bay of Somme (eastern English Channel, France). Continental Shelf Research 24, 14371449.CrossRefGoogle Scholar
Mock, T and Hoch, N (2005) Long-term temperature acclimation of photosynthesis in steady-state cultures of the polar diatom Fragilariopsis cylindrus. Photosynthesis Research 85, 307317.CrossRefGoogle ScholarPubMed
Morelle, J, Claquin, P and Orvain, F (2020) Evidence for better microphytobenthos dynamics in mixed sand/mud zones than in pure sand or mud intertidal flats (Seine estuary, Normandy, France). PLoS ONE 15, 124.CrossRefGoogle Scholar
Morris, EP and Kromkamp, JC (2003) Influence of temperature on the relationship between oxygen- and fluorescence-based estimates of photosynthetic parameters in a marine benthic diatom (Cylindrotheca closterium). European Journal of Phycology 38, 133142.CrossRefGoogle Scholar
Oliver, RL, Whittington, J, Lorenz, Z and Webster, IT (2003) The influence of vertical mixing on the photoinhibition of variable chlorophyll a fluorescence and its inclusion in a model of phytoplankton photosynthesis. Journal of Plankton Research 25, 11071129.CrossRefGoogle Scholar
Perkins, RG, Mouget, JL, Lefebvre, S and Lavaud, J (2006) Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic diatoms. Marine Biology 149, 703712.CrossRefGoogle Scholar
Pierre, G, Zhao, JM, Orvain, G, Dupuy, C, Klein, GL, Graber, M and Maugard, T (2014) Seasonal dynamics of extracellular polymeric substances (EPS) in surface sediments of a diatom-dominated intertidal mudflat (Marennes–Oléron, France). Journal of Sea Research 92, 2635.CrossRefGoogle Scholar
Pniewski, FF, Richard, P, Latała, A and Blanchard, G (2017) Non-photochemical quenching in epipsammic and epipelic microalgal assemblages from two marine ecosystems. Continental Shelf Research 136, 7482.CrossRefGoogle Scholar
Ralph, PJ and Gademann, R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany 82, 222237.CrossRefGoogle Scholar
Ribeiro, L, Brotas, V, Rincé, Y and Jesus, B (2013) Structure and diversity of intertidal benthic diatom assemblages in contrasting shores: a case study from the Tagus estuary. Journal of Phycology 49, 258270.CrossRefGoogle ScholarPubMed
Richardson, K, Beardall, J and Raven, JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytologist 93, 157191.CrossRefGoogle Scholar
Round, FE, Crawford, RM and Mann, DG (1990) Diatoms: Biology and Morphology of the Genera. Cambridge: Cambridge University Press, 747 pp.Google Scholar
Ruban, A, Lavaud, J, Rousseau, B, Guglielmi, G, Horton, P and Etienne, AL (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynthesis Research 82, 165.CrossRefGoogle ScholarPubMed
Salleh, S and McMinn, A (2011) The effects of temperature on the photosynthetic parameters and recovery of two temperate benthic diatom, Amphora cf. coffeaeformis and Cocconeis cf. sublittoralis (Bacillariophyceae). Journal of Phycology 47, 14131424.CrossRefGoogle Scholar
Scholz, B and Liebezeit, G (2012) Microphytobenthic dynamics in a Wadden Sea intertidal flat – Part I: seasonal and spatial variation of diatom communities in relation to macronutrient supply. European Journal of Phycology 47, 105119.CrossRefGoogle Scholar
Schreiber, U (2004) Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method. In Papageorgiou, G and Govindjee, (eds), Chlorophyll A Fluorescence: A Signature of Photosynthesis. Dordrecht: Kluwer Academic Publishers, pp. 279319.CrossRefGoogle Scholar
Serôdio, J, Coelho, H, Vieira, S and Cruz, S (2006) Microphytobenthos vertical migratory photoresponse as characterised by light-response curves of surface biomass. Estuarine, Coastal and Shelf Science 68, 547556.Google Scholar
Serôdio, J, Cruz, S, Vieira, S and Brotas, V (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. Journal of Experimental Marine Biology and Ecology 326, 157169.CrossRefGoogle Scholar
Torres, MA, Ritchie, RJ, Lilley, RMC, Grillet, C and Larkum, AWD (2014) Measurement of photosynthesis and photosynthetic efficiency in two diatoms. New Zealand Journal of Botany 52, 627.CrossRefGoogle Scholar
Underwood, GJC and Kromkamp, J (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Advances in Ecological Research 29, 93153.CrossRefGoogle Scholar
Vieira, S, Cartaxan, P, Máguas, C and Da Silva, JM (2016) Photosynthesis in estuarine intertidal microphytobenthos is limited by inorganic carbon availability. Photosynthesis Research 128, 8592.CrossRefGoogle ScholarPubMed
Vieira, S, Ribeiro, L, da Silva, JM and Cartaxana, P (2013) Effects of short-term changes in sediment temperature on the photosynthesis of two intertidal microphytobenthos communities. Estuarine. Coastal and Shelf Science 119, 112118.CrossRefGoogle Scholar
Walter, B, Peters, J, Van Beusekom, JEE and St. John, MA (2015) Interactive effects of temperature and light during deep convection: a case study on growth and condition of the diatom Thalassiosira weissflogii. ICES Journal of Marine Science 72, 20612071.CrossRefGoogle Scholar
Witkowski, A, Lange-Bertalot, H and Metzeltin, D (2000) In Lange-Bertalot H (ed.), Diatom Flora of Marine Coasts. Iconographia Diatomologica Vol. 7, 925 pp.Google Scholar
Wu, Y, Zhang, M, Li, Z, Xu, J and Beardall, J (2020) Differential responses of growth and photochemical performance of marine diatoms to ocean warming and high light irradiance. Photochemistry and Photobiology 96, 10741082.CrossRefGoogle ScholarPubMed
Xu, L, Wang, Q, Wu, S and Li, D (2014) Improvement of hydrogen yield of lba-transgenic Chlamydomonas reinhardtii caused by increasing respiration and impairing photosynthesis. International Journal of Hydrogen Energy 39, 1334713352.CrossRefGoogle Scholar
Yun, MS, Lee, SH and Chung, IK (2010) Photosynthetic activity of benthic diatoms in response to different temperatures. Journal of Applied Phycology 22, 559562.CrossRefGoogle Scholar
Zhang, X, Yuan, H, Guan, L, Wang, X, Wang, Y, Jiang, Z, Cao, L and Zhang, X (2019) Influence of photoperiods on microalgae biofilm: photosynthetic performance, biomass yield, and cellular composition. Energies 12, 37.Google Scholar
Supplementary material: Image

Salleh and McMinn supplementary material

Figure S1

Download Salleh and McMinn supplementary material(Image)
Image 1.9 MB
Supplementary material: Image

Salleh and McMinn supplementary material

Figure S2

Download Salleh and McMinn supplementary material(Image)
Image 1.9 MB