- 1School of Marine Sciences, Sun Yat-sen University, Zhuhai, China
- 2Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, China
Dissolved organic matter (DOM) in the ocean is a complexity with high diversity in chemical compositions. Diverse organic compounds are essential in global biogeochemical cycles composed of biogenic elements, mainly carbon, nitrogen, and sulfur (Carlson and Hansell, 2015). A certain fraction of DOM is light-absorbing, referred to as chromophoric DOM (CDOM). An important subset of CDOM is fluorescent, especially fluorescent DOM (FDOM) (Nelson and Siegel, 2013). CDOM absorbs UV–visible light with the typical absorption spectra in the blue and ultraviolet wavebands (200–400 nm and 400–800 m), and FDOM is in a generally limited window of excitation and emission wavelengths (240 nm−500 nm in excitation and 300–600 in emission) (Stedmon and Nelson, 2015). The optical properties of marine DOM were comparable and widely used in biogeochemistry, tracing the fate and source of DOM in the ocean (Coble, 2007). Wide distributions of marine FDOM were investigated across the global ocean (Yamashita and Tanoue, 2008; Nelson and Siegel, 2013). Based on studies from hydrography, high concentrations of CDOM/FDOM were normally investigated in riverine (Coble, 1996; Opsahl and Benner, 1997; Fellman et al., 2009) and soil samples (Guéguen and Cuss, 2011). Lignin is an essential and well-known terrestrial biomarker that also presents properties in absorbance and fluorescence (Hernes et al., 2009; Yamashita et al., 2015). However, the details of fluorescent signals of marine DOM were not able to mimic those from lignin or other terrestrial FDOM (Vecchio and Blough, 2004; Yamashita et al., 2010; Andrew et al., 2013), and the turnover rate of lignin and other terrestrial DOM could weakly support the standing stoke of marine FDOM (Opsahl and Benner, 1997; Hernes and Benner, 2003; Benner, 2004; Mannino et al., 2008; Yamashita et al., 2015). The debate about whether the origin of marine FDOM is autochthonous or allochthonous is ongoing (Drozdowska et al., 2015; Yamashita et al., 2015; Chen et al., 2016; Kwon et al., 2018). Sediment leaking would be supplementary to the allochthonous origin but limited to the wide distribution of marine FDOM (Skoog et al., 1996; Burdige et al., 2004; Yang et al., 2012; Chen et al., 2016). There must be another constant and generous autochthonous origin in the ocean. It is the black box generally called biogenetic derivation or, more precisely, the microbial origin, before our dissection on one of the key primary producers, picocyanobacteria (Zhao et al., 2017).
Microbes in the sea are diverse in terms of taxonomy and functional groups. Their activities are closely correlated with the fate of DOM (Tranvik, 1992; Jiao et al., 2010, 2011; Kujawinski, 2011). Cyanobacteria were unique among all these known autotrophic and heterotrophic microbes with phycobilin pigments (Chakdar and Pabbi, 2016; Saini et al., 2018). These tetrapyrrolic-based light-harvesting pigments were auto-fluorescent and in different types according to the peptides linked to the core tetrapyrrolic structure (Battersby, 2000; Stadnichuk et al., 2015). In the EEM analyses of DOM from picocyanobacterial cultures, the optical properties closely resembled typical oceanic FDOM found in the deep ocean. With a further comprehensive bulk analysis with the high-resolution mass spectrum and nuclear magnetism, the degradation products of phycobilin pigments were targeted to be the candidate that contributed to the fluorescent signal in picocyanobacterial-derived DOM. The dominant groups of unicellular picocyanobacteria, belonging to genera Synechococcus and Prochlorococcus, were widely distributed in the global ocean and contributed to up to 40% of primary production. Hence, picocyanobacteria were proved to be the very first certain contributor to marine FDOM (Zhao et al., 2017; Zheng et al., 2021). Even with a rough estimation based on the laboratory per cell production and total standing stokes of the picocyanobacterial populations, we could hardly define the proportion of picocyanobacterial-derived FDOM to the total oceanic FDOM without a global survey coupled with in-filed trace estimation.
Fluorescence is a specific optical property of compounds that is based on their particular chemical structure and composition. The optical properties are correlated to the molecular structures of organic compounds, with light absorption resulting in the loss of electron energy during transitions from the excited state to the ground state. Fluorophores are more specific than chromophores because fluorescence occurs only when the electron transitions from the lowest excited state. Structures such as aromatic and unsaturated bonds contribute to the majority of CDOM chromophores, but fluorescent signals are more unique and complex and are limited to certain compounds (Stedmon and Nelson, 2015). The diversity of microbial taxa and metabolic functions offers a broad range of selection opportunities for the production of organic compounds with fluorescent properties.
Picocyanobacteria could be essential contributors to marine FDOM (Xiao et al., 2021), but others are still lined up on the waiting list of potential candidates. Clues were gained from the initial study. Not all microbial species can produce fluorescent compounds without the cellular structure or metabolism function basics. Synechococcus released FDOM components when cells were lysed by either viral infection (Zhao et al., 2017, 2019) or environmental pressure (Zheng et al., 2021). The degradation products of the cell structure materials contributed directly to the FDOM signals (Lian et al., 2021). The photosynthetic pigment of Prochlorococcus was divinyl chlorophyll a and b (Chisholm et al., 1992), which was not the proved to be the origin of pyrrolic degradation products. Phycobilin genes were found in the Prochlorococcus genome, indicating the capacity of their production and further contribution (Steglich et al., 2005). Eukaryotic algae that contributed mainly to the DOM production in eutrophic zones would become the most competitive candidates. The absorbance of diatoms or dinoflagellate cultures was evaluated but no detailed fluorescent signals have been reported yet (Rochelle-Newall and Fisher, 2002; Burdige et al., 2004). Chlorophylls are a type of porphyrin compound that contains pyrrole rings, which are known to contribute to fluorescence (Zhao et al., 2017). However, chlorophylls are not readily water-soluble, so they are unlikely to directly contribute to FDOM in the ocean. The photosynthetic-related pigments in all kinds of microbes should be targeted first and foremost due to the chemical structure of fluorescent compounds (Kramer and Herndl, 2004). Candidates' range could be not only limited to the well-known photosynthetic algae groups but also photosynthetic prokaryotic microbes and other pigmented bacterial groups, such as the aerobic anoxygenic phototrophic bacteria (AAPB) (Yurkov and Beatty, 1998; Jiao et al., 2007; Ferrera et al., 2017) and proteorhodopsin in bacteria and archaea (Béjà et al., 2001; Frigaard et al., 2006; Gómez-Consarnau et al., 2007; DeLong and Béjà, 2010), and even in viruses (Yutin and Koonin, 2012).
Beyond the demonstration of the chemical nature, picocyanobacterial-derived FDOM was nitrogen-rich components in chemical compositions. The results led to a further discussion that FDOM could contribute importantly to both the organic carbon and nitrogen pools. The microbial origin of FDOM, e.g., picocyanobacteria, would be an essential link to coupling the nitrogen and carbon cycles in the ocean via DOM. The direction of the field was that modified estimations from laboratory incubation expanded to in situ quantification, filling the gaps in conceptual ameworks and models.
In conclusion, microbes were proven to be the key allochthonous origin of marine FDOM. On account of their high diversity, the verifications need to be more precise and focused. Combined application of multi-techniques is necessary for future attempts to further define the chemical nature of marine FDOM, in terms of the chemical composition and structure analyses of bulk DOM as well as the genome and transcriptome studies of microbial cell structure and metabolism.
Author contributions
The author confirms being the sole contributor of this work and has approved it for publication.
Funding
This study was supported by National Natural Science Foundation of China (Nos. 41906077 and 31970486), the National Natural Science Foundation of China-Guangdong Provincial Joint Fund Project (U1901209), Science and Technology Program of Guangzhou (No. 202002030453), and the Guangdong Basic and Applied Basic Research Foundation (2020A1515010908).
Acknowledgments
The author would like to thank Michael Gonisor from CBL, UMCES, USA and Hui Wang from Shantou University, China for the inspiration of these opinions and further collaborative research.
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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References
Andrew, A. A., Vecchio, R. D., Subramaniam, A., and Blough, N. V. (2013). Chromophoric dissolved organic matter (CDOM) in the Equatorial atlantic ocean: optical properties and their relation to CDOM structure and source. Mar. Chem. 148, 33–43. doi: 10.1016/j.marchem.2012.11.001
Battersby, A. R. (2000). Tetrapyrroles: the pigments of life. Nat. Prod. Rep. 17, 507–526. doi: 10.1039/b002635m
Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M., and DeLong, E. F. (2001). Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789. doi: 10.1038/35081051
Benner, R. (2004). What happens to terrestrial organic matter in the ocean? Mar. Chem. 92, 307–310. doi: 10.1016/j.marchem.2004.06.033
Burdige, D. J., Kline, S. W., and Chen, W. (2004). Fluorescent dissolved organic matter in marine sediment pore waters. Mar. Chem. 89, 289–311. doi: 10.1016/j.marchem.2004.02.015
Carlson, C. A., and Hansell, D. A. (2015). “DOM sources, sinks, reactivity, and budgets,” in Biogeochemistry of Marine Dissolved Organic Matter, Second Edition (Boston, MA: Academic Press), 65–126. doi: 10.1016/B978-0-12-405940-5.00003-0
Chakdar, H., and Pabbi, S. (2016). Frontier discoveries and innovations in interdisciplinary. Microbiology. 45–69. doi: 10.1007/978-81-322-2610-9_4
Chen, M., Kim, J. H., Nam, S. I., Niessen, F., Hong, W. L., Kang, M. H., et al. (2016). Production of fluorescent dissolved organic matter in Arctic Ocean sediments. Sci. Rep-UK 6, 39213. doi: 10.1038/srep39213
Chisholm, S. W., Frankel, S. L., Goericke, R., Olson, R. J., Palenik, B., Waterbury, J. B., et al. (1992). Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch. Microbiol. 157, 297–300. doi: 10.1007/BF00245165
Coble, P. G. (1996). Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar. Chem. 51, 325–346. doi: 10.1016/0304-4203(95)00062-3
Coble, P. G. (2007). Marine optical biogeochemistry: the chemistry of ocean color. Cheminform 38, 265. doi: 10.1002/chin.200720265
DeLong, E. F., and Béjà, O. (2010). The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times. PLoS Biol. 8, e1000359. doi: 10.1371/journal.pbio.1000359
Drozdowska, V., Kowalczuk, P., and Jozefowicz, M. (2015). Spectrofluorometric characteristics of fluorescent dissolved organic matter in a surface microlayer in the Southern Baltic coastal waters. J Eur. Opt. Soc. Rapid Publ. 10, 50. doi: 10.2971/jeos.2015.15050
Fellman, J. B., Hood, E., D'Amore, D. V., Edwards, R. T., and White, D. (2009). Seasonal changes in the chemical quality and biodegradability of dissolved organic matter exported from soils to streams in coastal temperate rainforest watersheds. Biogeochemistry 95, 277–293. doi: 10.1007/s10533-009-9336-6
Ferrera, I., Sánchez, O., Kolárová, E., KoblíŽek, M., and Gasol, J. M. (2017). Light enhances the growth rates of natural populations of aerobic anoxygenic phototrophic bacteria. ISME J. 11, 2391–2393. doi: 10.1038/ismej.2017.79
Frigaard, N-. U., Martinez, A., Mincer, T. J., and DeLong, E. F. (2006). Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847–850. doi: 10.1038/nature04435
Gómez-Consarnau, L., González, J. M., Coll-Lladó, M., Gourdon, P., Pascher, T., Neutze, R., et al. (2007). Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445, 210–213. doi: 10.1038/nature05381
Guéguen, C., and Cuss, C. W. (2011). Characterization of aquatic dissolved organic matter by asymmetrical flow field-flow fractionation coupled to UV–Visible diode array and excitation emission matrix fluorescence. J. Chromatogr. A. 1218, 4188–4198. doi: 10.1016/j.chroma.2010.12.038
Hernes, P. J., and Benner, R. (2003). Photochemical and microbial degradation of dissolved lignin phenols: Implications for the fate of terrigenous dissolved organic matter in marine environments. J. Geophys. Res. Oceans. 108, 1421. doi: 10.1029/2002JC001421
Hernes, P. J., Bergamaschi, B. A., Eckard, R. S., and Spencer, R. G. M. (2009). Fluorescence-based proxies for lignin in freshwater dissolved organic matter. J. Geophys. Res. Biogeosci. 114, 75. doi: 10.1029/2009JG000938
Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W., et al. (2010). Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599. doi: 10.1038/nrmicro2386
Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W., et al. (2011). Biosequestration of carbon by heterotrophic microorganisms. Nat. Rev. Microbiol. 9, 75–75. doi: 10.1038/nrmicro2386-c2
Jiao, N., Zhang, Y., Zeng, Y., Hong, N., Liu, R., Chen, F., et al. (2007). Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ. Microbiol. 9, 3091–3099. doi: 10.1111/j.1462-2920.2007.01419.x
Kramer, G., and Herndl, G. (2004). Photo- and bioreactivity of chromophoric dissolved organic matter produced by marine bacterioplankton. Aquat. Microb. Ecol. 36, 239–246. doi: 10.3354/ame036239
Kujawinski, E. B. (2011). The impact of microbial metabolism on marine dissolved organic matter. Annu. Rev. Mar. Sci. 3, 567–599. doi: 10.1146/annurev-marine-120308-081003
Kwon, H. K., Kim, G., Lim, W. A., and Park, J. W. (2018). In-situ production of humic-like fluorescent dissolved organic matter during Cochlodinium polykrikoides blooms. Estuar. Coast. Shelf Sci. 203, 119–126. doi: 10.1016/j.ecss.2018.02.013
Lian, J., Zheng, X., Zhuo, X., Chen, Y., He, C., Zheng, Q., et al. (2021). Microbial transformation of distinct exogenous substrates into analogous composition of recalcitrant dissolved organic matter. Environ. Microbiol. 23, 2389–2403. doi: 10.1111/1462-2920.15426
Mannino, A., Russ, M. E., and Hooker, S. B. (2008). Algorithm development and validation for satellite-derived distributions of DOC and CDOM in the U.S. Middle Atlantic Bight. J. Geophys Res. Oceans 113, 4493. doi: 10.1029/2007JC004493
Nelson, N. B., and Siegel, D. A. (2013). The global distribution and dynamics of chromophoric dissolved organic matter. Mar. Sci. 5, 447–476. doi: 10.1146/annurev-marine-120710-100751
Opsahl, S., and Benner, R. (1997). Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 386, 480–482. doi: 10.1038/386480a0
Rochelle-Newall, E. J., and Fisher, T. R. (2002). Production of chromophoric dissolved organic matter fluorescence in marine and estuarine environments: an investigation into the role of phytoplankton. Mar. Chem. 77, 7–21. doi: 10.1016/S0304-4203(01)00072-X
Saini, D. K., Pabbi, S., and Shukla, P. (2018). Cyanobacterial pigments: perspectives and biotechnological approaches. Food Chem. Toxicol. 120, 616–624. doi: 10.1016/j.fct.2018.08.002
Skoog, A., Hall, P. O. J., Hulth, S., Paxéus, N., Loeff, M. R. V. D., Westerlund, S., et al. (1996). Early diagenetic production and sediment-water exchange of fluorescent dissolved organic matter in the coastal environment. Geochim. Cosmochim. Ac. 60, 3619–3629. doi: 10.1016/0016-7037(96)83275-3
Stadnichuk, I. N., Krasilnikov, P. M., and Zlenko, D. V. (2015). Cyanobacterial phycobilisomes and phycobiliproteins. Microbiology+ 84, 101–111. doi: 10.1134/S0026261715020150
Stedmon, C. A., and Nelson, N. B. (2015). “The optical properties of DOM in the ocean,” in Biogeochemistry of marine dissolved organic matter. Academic Press., pp. 481–508. doi: 10.1016/B978-0-12-405940-5.00010-8
Steglich, C., Frankenberg-Dinkel, N., Penno, S., and Hess, W. R. (2005). A green light-absorbing phycoerythrin is present in the high-light-adapted marine cyanobacterium Prochlorococcus sp. MED4. Environ. Microbiol. 7, 1611–1618. doi: 10.1111/j.1462-2920.2005.00855.x
Tranvik, L. J. (1992). Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept of the microbial loop. Hydrobiologia 229, 107–114. doi: 10.1007/BF00006994
Vecchio, R. D., and Blough, N. V. (2004). Spatial and seasonal distribution of chromophoric dissolved organic matter and dissolved organic carbon in the Middle Atlantic Bight. Mar. Chem. 89, 169–187. doi: 10.1016/j.marchem.2004.02.027
Xiao, X., Guo, W., Li, X., Wang, C., Chen, X., Lin, X., et al. (2021). Viral lysis alters the optical properties and biological availability of dissolved organic matter derived from prochlorococcus picocyanobacteria. Appl. Environ. Microb. 87, 20. doi: 10.1128/AEM.02271-20
Yamashita, Y., Cory, R. M., Nishioka, J., Kuma, K., Tanoue, E., Jaffé, R., et al. (2010). Fluorescence characteristics of dissolved organic matter in the deep waters of the Okhotsk Sea and the northwestern North Pacific Ocean. Deep Sea Res. Part Ii Top Stud. Oceanogr. 57, 1478–1485. doi: 10.1016/j.dsr2.2010.02.016
Yamashita, Y., Fichot, C. G., Shen, Y., Jaffé, R., and Benner, R. (2015). Linkages among fluorescent dissolved organic matter, dissolved amino acids and lignin-derived phenols in a river-influenced ocean margin. Front. Mar. Sci. 2, 92. doi: 10.3389/fmars.2015.00092
Yamashita, Y., and Tanoue, E. (2008). Production of bio-refractory fluorescent dissolved organic matter in the ocean interior. Nat. Geosci. 1, 579–582. doi: 10.1038/ngeo279
Yang, L., Hong, H., Guo, W., Chen, C. T. A., Pan, P-. I., Feng, C-. C., et al. (2012). Absorption and fluorescence of dissolved organic matter in submarine hydrothermal vents off NE Taiwan. Mar. Chem. 128, 64–71. doi: 10.1016/j.marchem.2011.10.003
Yurkov, V. V., and Beatty, J. T. (1998). Aerobic anoxygenic phototrophic bacteria. Microbiol. Mol. Biol. R 62, 695–724. doi: 10.1128/MMBR.62.3.695-724.1998
Yutin, N., and Koonin, E. V. (2012). Proteorhodopsin genes in giant viruses. Biol. Direct. 7, 34. doi: 10.1186/1745-6150-7-34
Zhao, Z., Gonsior, M., Luek, J., Timko, S., Ianiri, H., Hertkorn, N., et al. (2017). Picocyanobacteria and deep-ocean fluorescent dissolved organic matter share similar optical properties. Nat. Commun. 8, 15284. doi: 10.1038/ncomms15284
Zhao, Z., Gonsior, M., Schmitt-Kopplin, P., Zhan, Y., Zhang, R., Jiao, N., et al. (2019). Microbial transformation of virus-induced dissolved organic matter from picocyanobacteria: coupling of bacterial diversity and DOM chemodiversity. ISME J. 1–15. doi: 10.1038/s41396-019-0449-1
Keywords: marine microbes, FDOM's source, marine organic nitrogen, marine organic carbon, microbial pigments
Citation: Zhao Z (2023) The microbial origin of marine autochthonous fluorescent dissolved organic matter. Front. Microbiol. 14:1152795. doi: 10.3389/fmicb.2023.1152795
Received: 28 January 2023; Accepted: 15 March 2023;
Published: 12 April 2023.
Edited by:
Dengzhou Gao, East China Normal University, ChinaCopyright © 2023 Zhao. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Zhao Zhao, emhhb3poYW81JiN4MDAwNDA7bWFpbC5zeXN1LmVkdS5jbg==