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Bacterial consumption of total and dissolved organic carbon in the Great Barrier Reef

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Abstract

Heterotrophic bacteria typically take up directly dissolved organic matter due to the small molecular size, although both particulate and dissolved organic matter have labile (easily consumed) compounds. Tropical coastal waters are important ecosystems because of their high productivity. However, few studies have determined bacterial cycling (i.e. carbon uptake by bacteria and allocation for bacterial biomass and respiration) of dissolved organic carbon in coastal tropical waters, and none has determined bacterial cycling of total and dissolved organic carbon simultaneously. In this study we followed bacterial biomass and production, and organic carbon changes over short-term (12 days) dark incubations with (total organic carbon, TOC) and without particulate organic carbon additions (dissolved organic carbon, DOC). The study was performed at three sites along the middle stretch of the Great Barrier Reef (GBR) during the dry and wet seasons. Our results show that the bacterial growth efficiency is low (0.1–11.5%) compared to other coastal tropical systems, and there were no differences in the carbon cycling between organic matter sources, seasons or locations. Nonetheless, more carbon was consumed in the TOC compared to the DOC incubations, although the proportion allocated to biomass and respiration was similar. This suggests that having more bioavailable substrate in the particulate form did not benefit bacteria. Overall, our study indicates that when comparing the obtained respiration rates with previously measured primary production rates, the GBR is a heterotrophic system. More detailed studies are required to fully explore the mechanisms used by bacteria to cycle TOC and DOC in tropical coastal waters.

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Abbreviations

BA:

Bacterial abundance

BB:

Bacterial biomass

BDOC:

Bioavailable DOC

BGE:

Bacterial growth efficiency

BP:

Bacterial production

BCD:

Bacterial carbon demand

Cell BP:

Cell specific bacterial production

DOC:

Dissolved organic carbon

DOM:

Dissolved organic matter

OM:

Organic matter

POC:

Particulate organic carbon

POM:

Particulate organic matter

TOC:

Total organic carbon

TOM:

Total organic matter

References

  • Alongi DM, Patten NL, McKinnon D, Köstner N, Bourne DG, Brinkman R (2015) Phytoplankton, bacterioplankton and virioplankton structure and function across the southern Great Barrier Reef shelf. J Mar Syst 142:25–39

    Google Scholar 

  • Amato P, Doyle SM, Battista JR, Christner BC (2010) Implications of subzero metabolic activity on long-term microbial survival in terrestrial and extraterrestrial permafrost. Astrobiology 10(8):789

    Google Scholar 

  • Antai EE, Asitok AD, Paul A (2013) Bacterial growth efficiency, respiration and secondary production and in the cross river estuary, Nigeria and the near coast. Int J Sci Res 4(10):1791–1798

    Google Scholar 

  • Apple JK, Giorgio PAd (2007) Organic substrate quality as the link between bacterioplankton carbon demand and growth efficiency in a temperate salt-marsh estuary. ISME J 1:729–742

    Google Scholar 

  • Arnosti C, Repeta DJ (1994) Extracellular enzyme activity in anaerobic bacterial cultures evidence of pullulanase activity among mesophilic marine bacteria. Appl Environ Microbiol 60:840–846

    Google Scholar 

  • Bauer JE, Druffel ERM (1998) Oceanmargins as a significant source of organicmatter to the deep open ocean. Nature 392(6675):482–485

    Google Scholar 

  • Brunskill GJ (2010) Tropical margins. In: Liu K-K, Atkinson L, Talaue-McManus L (eds) Carbon and nutrient fluxes in continental margins. Global change—the IGBP series. Springer, Heidelberg, pp 423–493

    Google Scholar 

  • Brussaard CP, Wilhelm SW, Thingstad F, Weinbauer MG, Bratbak G, Heldal M, Kimmance SA, Middelboe M, Nagasaki K, Paul JH, Schroeder DC, Suttle CA, Vaqué D, Wommack KE (2008) Global-scale processes with a nanoscale drive: the role of marine viruses. ISME J 2:575–578

    Google Scholar 

  • Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, Otero MP, Vergin K, Wheeler BR (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30:19–36

    Google Scholar 

  • Cherrier J, Bauer JE, Druffel ERM (1996) Utilization and turnover of labile dissolved organic matter by bacterial heterotrophs in eastern North Pacific surface waters. Mar Ecol Prog Ser 139:267–279

    Google Scholar 

  • Cuskin F, Lowe EC, Temple MJ, Zhu Y, Cameron EA, Pudlo NA, Porter NT, Urs K, Thompson AJ, Cartmell A, Rogowski A, Hamilton BS, Chen R, Tolbert TJ, Piens K, Bracke D, Vervecken W, Hakki Z, Speciale G, Munōz-Munōz JL, Day A, Peña MJ, McLean R, Suits MD, Boraston AB, Ziemer TACJ, Williams SJ, Davies GJ, Abbott DW, Martens EC, Gilbert HJ (2015) Human gut bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517:165–186

    Google Scholar 

  • Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Google Scholar 

  • Eppley RW, Peterson BJ (1979) Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282:677–680

    Google Scholar 

  • Fagerbakke KM, Heldal M, Norland S (1996) Content of carbon, nitrogen, oxygen, sulphur and phosphorus in native aquatic and cultured bacteria. Aquat Microb Ecol 10:15–27

    Google Scholar 

  • Fuhrman JA, Azam F (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl Environ Microbiol 36:1085–1095

    Google Scholar 

  • Furnas M, Mitchell A, Skuza M, Brodie J (2005) In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar Pollut Bull 51:253–265

    Google Scholar 

  • Furnas M, Alongi D, McKinnon D, Trott L, Skuza M (2011) Regional-scale nitrogen and phosphorus budgets for the northern (14°S) and central (17°S) Great Barrier Reef shelf ecosystem. Cont Shelf Res 31(19–20):1967–1990

    Google Scholar 

  • Garber JH (1984) Laboratory study of nitrogen and phosphorus remineralization during the decomposition of coastal plankton and seston. Estuar Coast Shelf Sci 18:685–702

    Google Scholar 

  • Gasol JM, Morán XAG (2015) Flow cytometric determination of microbial abundances and its use to obtainindices of community structure and relative activity. In: McGenity TJ, Timmis KN, Nogales B (eds) Hydrocarbon and lipid microbiology protocols. Springer, Heidelberg, pp 159–187

    Google Scholar 

  • Gasol JM, Pinhassi J, Alonso-Sáez L, Ducklow H, Herndl GJ, Koblizek M, Labrenz M, Luo Y, Morán XAG, Reinthaler T, Simon M (2008) Towards a better understanding of microbial carbon flux in the sea. Aquat Microb Ecol 53:21–38

    Google Scholar 

  • Giorgio PAd, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Google Scholar 

  • González N, Anadón R, Viesca L (2003) Carbon flux through the microbial community in a temperate sea during summer: role of bacterial metabolism. Aquat Microb Ecol 33:117–126

    Google Scholar 

  • González-Benítez N, García-Corral LS, Morán XAG, Middelburg JJ, Pizay MD, Gattuso JP (2019) Drivers of microbial carbon fluxes variability in two oligotrophic Mediterranean coastal systems. Sci Rep 9:17669

    Google Scholar 

  • Guenther M, Paranhos R, Rezende CE, Gonzalez-Rodriguez E, Valentin JL (2008) Dynamics of bacterial carbon metabolism at the entrance of a tropical eutrophic bay influenced by tidal oscillation. Aquat Microb Ecol 50:123–133

    Google Scholar 

  • Guenther M, Gonzalez-Rodriguez E, Flores-Montes M, Araújo M, Neumann-Leitão S (2017) High bacterial carbon demand and low growth efficiency at a tropical hypereutrophic estuary: importance of dissolved organic matter remineralization. Braz J Oceanogr 65(3):382–391

    Google Scholar 

  • Hammes F, Vital M, Egli T (2010) Critical evaluation of the volumetric “bottle effect” on the microbial batch growth. Appl Environ Microbiol 76(4):1278–1281

    Google Scholar 

  • Hansen HP, Koroleff F (1999) Automated chemical analysis. In: Grasshoff K, Krembling K, Ehrhardt M (eds) Methods of seawater analysis. Wiley, Hoboken, pp 159–226

    Google Scholar 

  • Hopley D, Smithers SG, Parnell K (2007) The geomorphology of the Great Barrier Reef: development, diversity and change. Cambridge Univ. Press, Cambridge

    Google Scholar 

  • Huete-Stauffer TM, Arandia-Gorostidi N, González-Benítez N, Díaz-Pérez L, Calvo-Díaz A, Morán XAG (2017) Large plankton enhance heterotrophy under experimental warming in a temperate coastal ecosystem. Ecosystems 21:1139–1154

    Google Scholar 

  • Lee CW, Bong CW, Hii YS (2009) Temporal variation of bacterial respiration and growth efficiency in tropical coastal waters. Appl Environ Microbiol 75(24):7594–7601

    Google Scholar 

  • Lønborg C, Alvarez-Salgado XA (2012) Recycling versus export of bioavailable dissolved organic matter in the coastal ocean and efficiency of the continental shelf pump. Glob Biogeochem Cycles 26:GB3018

    Google Scholar 

  • Lønborg C, Martínez-García S, Teira E, Álvarez-Salgado XA (2011) Bacterial carbon demand and growth efficiency in a coastal upwelling system. Aquat Microb Ecol 63:183–191

    Google Scholar 

  • Lønborg C, Devlin M, Waterhouse J, Brinkman R, Costello P, Silva Ed, Davidson J, Gunn K, Logan M, Petus C, Skuza BSM, Tonin H, Tracey D, Wright M, Zagorskis I (2016) Marine monitoring program: annual report for inshore water quality monitoring 2014 to 2015. Report for the Great Barrier Reef Marine Park Authority. Australian Institute of Marine Science and JCU TropWATER, Townsville, p 229

    Google Scholar 

  • Lønborg C, Nieto-Cid M, Hernando-Morales V, Hernandez-Ruiz M, Teira E, Álvarez-Salgado XA (2016) Photochemical alteration of dissolved organic matter and the subsequent effects on bacterial carbon cycling and diversity. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw048

    Article  Google Scholar 

  • Lønborg C, Doyle J, Furnas M, Menendez P, Benthuysen JA, Carreira C (2017) Seasonal organic matter dynamics in the Great Barrier Reef lagoon: Contribution of carbohydrates and proteins. Cont Shelf Res 138:95–105

    Google Scholar 

  • Lønborg C, Álvarez-Salgado XA, Duggan S, Carreira C (2018) Organic matter bioavailability in tropical coastal waters: The Great Barrier Reef. Limnol Oceanogr 63(2):1015–1035

    Google Scholar 

  • Lønborg C, Baltar F, Carreira C, Morán XAG (2019) Dissolved organic carbon source influences tropical coastal heterotrophic bacterioplankton response to experimental warming. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02807/full

    Article  Google Scholar 

  • Lønborg C, Calleja M, Fabricius K, Smith J (2019) The Great Barrier Reef: a source of CO2 to the atmosphere. Mar Chem 210:24–43

    Google Scholar 

  • Lønborg C, Carreira C, Jickells T, Álvarez-Salgado XA (2020) Impacts of global change on ocean dissolved organic carbon (DOC) cycling. Front Mar Sci 7:1–24

    Google Scholar 

  • McKinnon AD, Logan M, Castine SA, Duggan S (2013) Pelagic metabolism in the waters of the Great Barrier Reef. Limnol Oceanogr 58:1227–1242

    Google Scholar 

  • McKinnon AD, Duggan S, Logan M, Lønborg C (2017) Plankton respiration, production, and trophic state in tropical coastal and shelf waters adjacent to Northern Australia. Front Mar Sci. https://doi.org/10.3389/fmars.2017.00346

    Article  Google Scholar 

  • Morán XAG, Baltar F, Carreira C, Lønborg C (2020) Responses of physiological groups of tropical heterotrophic bacteria to temperature and dissolved organic matter additions: food matters more than warming. Environ Microbiol 22(5):1930–1943

    Google Scholar 

  • Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 121–152

    Google Scholar 

  • Nieuwenhuize J, Maas YEM, Middelburg JJ (1994) Rapid analysis of organic carbon and nitrogen in particulate materials. Mar Chem 45:217–224

    Google Scholar 

  • Pinhassi J, Gomez-Consarnau L, Alonso-Sáez L, Sala MM, Vidal M, Pedros-Alió C, Gasol JM (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241–252

    Google Scholar 

  • Ram ASP, Nair S, Chandramohan D (2003) Bacterial growth efficiency in the tropical estuarine and coastal waters of Goa, southwest coast of India. Microb Ecol 45:88–96

    Google Scholar 

  • Ram ASP, Nair S, Chandramohan D (2007) Bacterial growth efficiency in a tropical estuary: seasonal variability bubsidized by allochthonous carbon. Microb Ecol 53:591

    Google Scholar 

  • Rivkin RB, Anderson MR (1997) Inorganic nutrient limitation of oceanic bacterioplankton. Limnol Oceanogr 42:730–740

    Google Scholar 

  • Rivkin RB, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400

    Google Scholar 

  • Robinson C (2008) Heterotrophic bacterial respiration. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, Hoboken, pp 299–334

    Google Scholar 

  • Silva L, Calleja ML, Huete-Stauffer TM, Ivetic S, Ansari MI, Viegas M, Morán XAG (2019) Low abundances but high growth rates of coastal heterotrophic bacteria in the Red Sea. Front Microbiol 9:1–15

    Google Scholar 

  • Smith DC, Simon M, Allldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139–142

    Google Scholar 

  • Stewart FJ, Dalsgaard T, Young CR, Thamdrup B, Revsbech NP, Ulloa O, Canfield DE, Delong EF (2012) Experimental incubations elicit profound changes in community transcription in OMZ bacterioplankton. PLoS ONE 7(5):e37118

    Google Scholar 

  • Thingstad TF, Øvreås L, Egge JK, Løvdal T, Heldal M (2005) Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecol Lett 8(7):675–682

    Google Scholar 

  • Weiss MS, Abele U, Weckesser J, Welte W, Schiltz E, Schulz GE (1991) Molecular architecture and electrostatic properties of a bacterial porin. Science 254:1627–1630

    Google Scholar 

  • Wolanski E (1994) Physical oceanographic processes of the Great Barrier Reef. CRC Press, Boca Raton

    Google Scholar 

  • Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Res Oceanogr Abstr 10:221–231

    Google Scholar 

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Acknowledgements

We thank the crew of the R.V. Cape Ferguson for help at sea. The help of the Cruise leader (Irena Zagorskis) and other participants (Paul Costello and Johnstone Davidson) in obtaining the field data is also acknowledged. Two anonymous reviewers are also acknowledged for their constructive comments that improved substantially the quality of this manuscript.

Funding

Financial support for this study was provided by the Australian Institute of Marine Science. The field data included in the manuscript was obtained with support from the Great Barrier Reef Marine Park Authority, through funding from the Australian Government Reef Program and from the Australian Institute of Marine Science. Thanks are due to FCT/MCTES for the financial support to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds. CC was supported by Fundação para a Ciência e a Tecnologia (FCT; SFRH/BPD/117746/2016).

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Authors and Affiliations

  1. ECOMARE, CESAM-The Centre for Environmental and Marine Studies, University of Aveiro, Campus de Santiago, Aveiro, Portugal

    Cátia Carreira

  2. Department of Environmental Science, Aarhus University, 4000, Roskilde, Denmark

    Cátia Carreira

  3. Australian Institute of Marine Science, PMB No 3, Townsville, QLD, Australia

    Sam Talbot & Christian Lønborg

  4. Section for Applied Marine Ecology and Modelling, Department of Bioscience, Aarhus University, Aarhus, Denmark

    Christian Lønborg

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  1. Cátia Carreira
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Correspondence to Cátia Carreira.

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Carreira, C., Talbot, S. & Lønborg, C. Bacterial consumption of total and dissolved organic carbon in the Great Barrier Reef. Biogeochemistry 154, 489–508 (2021). https://doi.org/10.1007/s10533-021-00802-x

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