last updated 2023-09-05

The pelagic zone occupies approximately 1.3 billion km3 (1). Moreover, these aquatic environments hold a large biodiversity, most of it in the form of uncultivated planktonic microorganisms (2-5). This vast pelagic microbial biodiversity is essential to planetary health (6). They have heavily influenced biogeochemical cycles for at least a billion years (7). Moreover, their long-term co-evolutionary history has led, in many cases, to reduced genome size (3) which leaves pelagic microorganisms depending on interactions with other organisms. This makes the study of their ecology relevant to update fluxes in biogeochemical cycles (8), to update climate models (6), to design biotechnological tools that are more robust (9) among others. Our research plans and vision include four main topics:

1. Topic one: Interactions and dependencies on the pelagic microbial world

Aquatic microorganisms and their complex ecological interactions (Figure 1) are responsible for fixing about half of the carbon dioxide on Earth (10-12). Among microbial interactions, auxotrophies are important and yet key questions about them remain unanswered. Auxotrophy is defined as the inability to produce an essential metabolite (13). As environmental microorganisms evolved auxotrophies, they also developed dependencies and division of labor (14, 15). This untapped ecological knowledge has significant potential applications in biotechnology.

Figure 1. In this simplified scheme, different taxa are represented with different colors and are responsible for the transformation of carbon. Moreover, these different taxa interact through production of essential metabolites for which some other taxa are auxotrophic. One of the aims of my research is to understand the microbial interaction networks in the carbon cycle through auxotrophies and essential metabolites.

Microorganisms offer a number of advantages for testing social evolution theory (16). Our research topic tackles the question of how pelagic microorganisms interact as communities directly in their natural environment. Investigating the microbial interactions on naturally occurring microbial assemblages is of great importance to understand ecosystem functioning and to be able to use the principles in future biotechnological designs. Part of our reserach integrates innovative approaches (17): (i) a holistic exploration such as full community analysis of environmental samples, (ii) a reductionist approach, such as a physiological experiments in pure cultures, and finally (iii) model communities in culture or natural cohorts of microorganisms as an intermediate approach bridging holistic and reductionist approaches. In our research group, we will validate the patterns observed in nature through full community metagenomic studies, by doing fitness test in model communities and synthetic communities

2. Topic two: Patterns of biogeography of abundant aquatic microorganisms, including micro-diversity and co-evolution of abundant lineages.

Through the analysis of large metagenomic datasets in time-series or multi-geographic characteristics, we aim to answer questions regarding ecology and evolution across time and space.

3. Topic three: Key microbial players in the carbon and nitrogen cycle of aquatic environments.

In an era of increasing anthropogenic greenhouse gas emissions, decreasing food security and increasing need for clean energy sources, understanding the carbon cycle is crucial and relevant (Figure 2). Aquatic microorganisms are one of the largest contributors to carbon and nitrogen fixation in the atmosphere (20, 28, 29). However, the biogeochemical cycles have been severely affected by a new agent for change: humans. It is time for humans to seek and understand the balance that microorganisms brought to Earth and to take a hold of their rich biodiversity to build a sustainable green bioeconomy (30, 31).

Figure 2. Integration of all research topics and vision. Carbon cycle in aquatic environments linked through microbial interactions. The importance of primary producers and the flux of carbon between them and the heterotrophs. The vision of the scientific knowledge gained through the difference scientific topics, leading to applied research in the future in biotechnology. The Global goals reached through the research.

4. Topic four: Learn the fundamentals of microbial ecology and evolution that can lead to the improvement of biotechnological tools

One ambition long term is that all the ecological concepts and the cultures of cyanobacteria obtained in the research topics 1 and 3 will eventually lead to the development of better biotechnological tools (9). I strongly believe that our oceans and our lakes hold wisdom in their pelagic microorganisms that we can harvest to build a bioeconomy that is sustainable


1.         Costello MJ, Cheung A, De Hauwere N. Surface area and the seabed area, volume, depth, slope, and topographic variation for the world’s seas, oceans, and countries. Environ Sci Technol. 2010;44(23):8821-8.
2.         Menden-Deuer S, Rowlett J. Many ways to stay in the game: individual variability maintains high biodiversity in planktonic microorganisms. J R Soc Interface. 2014;11(95):20140031.
3.         Rodriguez-Gijon A, Nuy JK, Mehrshad M, Buck M, Schulz F, Woyke T, et al. A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy. Frontiers in microbiology. 2021;12:761869.
4.         Steen AD, Crits-Christoph A, Carini P, DeAngelis KM, Fierer N, Lloyd KG, et al. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 2019;13(12):3126-30.
5.         Del Campo J, Guillou L, Hehenberger E, Logares R, Lopez-Garcia P, Massana R. Ecological and evolutionary significance of novel protist lineages. European journal of protistology. 2016;55(Pt A):4-11.
6.         Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nature reviews Microbiology. 2019;17(9):569-86.
7.         Sanchez-Baracaldo P, Bianchini G, Wilson JD, Knoll AH. Cyanobacteria and biogeochemical cycles through Earth history. Trends Microbiol. 2022;30(2):143-57.
8.         Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat Microbiol. 2018;3(7):754-66.
9.         Giri S, Shitut S, Kost C. Harnessing ecological and evolutionary principles to guide the design of microbial production consortia. Curr Opin Biotechnol. 2020;62:228-38.
10.      Jardillier L, Zubkov MV, Pearman J, Scanlan DJ. Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME J. 2010;4(9):1180-92.
11.      Falkowski PG, Fenchel T, Delong EF. The Microbial Engines That Drive Earth’s Biogeochemical Cycles. Science. 2008;320(5879):1034-9.
12.      Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 2016;7:13219.
13.      Droop MR. Auxotrophy and organic compounds in the nutrition of marine phytoplankton. J gen Microbiol. 1957;16:286-93.
14.      Zengler K, Zaramela LS. The social network of microorganisms – how auxotrophies shape complex communities. Nature reviews Microbiology. 2018;16(6):383-90.
15.      Pacheco AR, Moel M, Segre D. Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems. Nat Commun. 2019;10.
16.      Ross-Gillespie A, Gardner A, West SA, Griffin AS. Frequency dependence and cooperation: theory and a test with bacteria. American Naturalist. 2007;170(3):331-42.
17.      Tecon R, Mitri S, Ciccarese D, Or D, van der Meer JR, Johnson DR. Bridging the Holistic-Reductionist Divide in Microbial Ecology. Msystems. 2019;4(1).
18.      Buck M, Garcia SL, Fernandez L, Martin G, Martinez-Rodriguez GA, Saarenheimo J, et al. Comprehensive dataset of shotgun metagenomes from oxygen stratified freshwater lakes and ponds. Sci Data. 2021;8(1):131.
19.      Rodriguez-Gijon A, Buck M, Andersson AF, Izabel-Shen D, Nascimento FJA, Garcia SL. Linking prokaryotic genome size variation to metabolic potential and environment. ISME Commun. 2023;3(1):25.
20.      Delmont TO, Quince C, Shaiber A, Esen OC, Lee ST, Rappe MS, et al. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat Microbiol. 2018;3(7):804-13.
21.      Garcia SL. Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions. Aquatic Microbial Ecology. 2016;77(2):79-85.
22.      Garcia SL, Buck M, Hamilton JJ, Wurzbacher C, Grossart HP, McMahon KD, et al. Model Communities Hint at Promiscuous Metabolic Linkages between Ubiquitous Free-Living Freshwater Bacteria. mSphere. 2018;3(3):103838.
23.      Mondav R, Bertilsson S, Buck M, Langenheder S, Lindstrom ES, Garcia SL. Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts. mSystems. 2020;5(5).
24.      Preussger D, Giri S, Muhsal LK, Ona L, Kost C. Reciprocal Fitness Feedbacks Promote the Evolution of Mutualistic Cooperation. Current biology : CB. 2020;30:1-11.
25.      Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, et al. A new view of the tree of life. Nature Microbiology. 2016;1(5):16048.
26.      Becker JW, Hogle SL, Rosendo K, Chisholm SW. Co-culture and biogeography of Prochlorococcus and SAR11. ISME J. 2019;13(6):1506-19.
27.      Rodriguez RL, Tsementzi D, Luo C, Konstantinidis KT. Iterative subtractive binning of freshwater chronoseries metagenomes identifies over 400 novel species and their ecologic preferences. Environ Microbiol. 2020;22(8):3394-412.
28.      Bar-On YM, Phillips R, Milo R. The biomass distribution on Earth. PNAS. 2018;115(25):6506-11.
29.      Peura S, Buck M, Aalto SL, Morales SE, Nykanen H, Eiler A. Novel autotrophic organisms contribute significantly to the internal carbon cycling potential of a boreal lake. Mbio. 2018;9(4):e00916-18.
30.      D’Amato D, Droste N, Allen B, Kettunen M, Lähtinen K, Korhonen J, et al. Green, circular, bio economy: A comparative analysis of sustainability avenues. Journal of Cleaner Production. 2017;168:716-34.
31.      Ducklow H. Microbial services: challenges for microbial ecologists in a changing world. Aquatic Microbial Ecology. 2008;53:13-9.
32.      Prosser JI, Martiny JBH. Conceptual challenges in microbial community ecology. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 2020;375(1798):20190241.
33.      Garcia SL, Buck M, McMahon KD, Grossart HP, Eiler A, Warnecke F. Auxotrophy and intrapopulation complementary in the “interactome’ of a cultivated freshwater model community. Molecular ecology. 2015;24(17):4449-59.
34.      Zubkov MV. Faster growth of the major prokaryotic versus eukaryotic CO2 fixers in the oligotrophic ocean. Nat Commun. 2014;5:3776.
35.      Azam F. OCEANOGRAPHY: Microbial Control of Oceanic Carbon Flux: The Plot Thickens. Science. 1998;280(5364):694-6.
36.      Ferrer-Gonzalez FX, Widner B, Holderman NR, Glushka J, Edison AS, Kujawinski EB, et al. Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy. ISME J. 2021;15(3):762-73.
37.      Patriarca C, Balderrama A, Moze M, Sjoberg PJR, Bergquist J, Tranvik LJ, et al. Investigating the Ionization of Dissolved Organic Matter by Electrospray. Analytical chemistry. 2020;92(20):14210-8.
38.      Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, et al. The global carbon cycle: a test of our knowledge of earth as a system. Science. 2000;290(5490):291-6.
39.      Hansell D, Carlson C, Repeta D, Schlitzer R. Dissolved Organic Matter in the Ocean: A Controversy Stimulates New Insights. Oceanography. 2009;22(4):202-11.
40.      Koch BP, Ludwichowski K-U, Kattner G, Dittmar T, Witt M. Advanced characterization of marine dissolved organic matter by combining reversed-phase liquid chromatography and FT-ICR-MS. Marine Chemistry. 2008;111(3-4):233-41.
41.      Amon RMW, Benner R. Bacterial utilization of different size classes of dissolved organic matter. Limnology and Oceanography. 1996;41(1):41-51.
42.      Koehler B, von Wachenfeldt E, Kothawala D, Tranvik LJ. Reactivity continuum of dissolved organic carbon decomposition in lake water. Journal of Geophysical Research: Biogeosciences. 2012;117(G1).
43.      Maki K, Kim C, Yoshimizu C, Tayasu I, Miyajima T, Nagata T. Autochthonous origin of semi-labile dissolved organic carbon in a large monomictic lake (Lake Biwa): carbon stable isotopic evidence. Limnology. 2009;11(2):143-53.
44.      Patriarca C, Sedano‐Núñez VT, Garcia SL, Bergquist J, Bertilsson S, Sjöberg PJR, et al. Character and environmental lability of cyanobacteria‐derived dissolved organic matter. Limnology and Oceanography. 2020;66(2):496-509.
45.      Moran MA, Ferrer‐González FX, Fu H, Nowinski B, Olofsson M, Powers MA, et al. The Ocean’s labile DOC supply chain. Limnology and Oceanography. 2022;67(5):1007-21.
46.      Fenchel T. The microbial loop – 25 years later. Journal of Experimental Marine Biology and Ecology. 2008;366(1-2):99-103.
47.      Gobler CJ. Climate Change and Harmful Algal Blooms: Insights and perspective. Harmful Algae. 2020;91:101731.
48.      Xu H, Paerl HW, Qin B, Zhu G, Gaoa G. Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography. 2010;55(1):420-32.
49.      Chen MY, Teng WK, Zhao L, Hu CX, Zhou YK, Han BP, et al. Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation. ISME J. 2021;15(1):211-27.
50.      Garcia SL, Nuy JK, Mehrshad M, Hampel JJ, Sedano-Núñez VT, Buck M, et al. Taxonomic and functional diversity of aquatic heterotrophs is sustained by dissolved organic matter chemodiversity. bioRxiv. 2022.