Unlocking the Genomic Taxonomy of the Prochlorococcus Collective

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MICROBIOLOGY OF AQUATIC SYSTEMS

Unlocking the Genomic Taxonomy of the Prochlorococcus Collective Diogo Tschoeke 1 & Vinicius W. Salazar 1 & Livia Vidal 1 & Mariana Campeão 1 & Jean Swings 1,2 & Fabiano Thompson 1 & Cristiane Thompson 1 Received: 13 February 2020 / Accepted: 7 May 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Prochlorococcus is the most abundant photosynthetic prokaryote on our planet. The extensive ecological literature on the Prochlorococcus collective (PC) is based on the assumption that it comprises one single genus comprising the species Prochlorococcus marinus, containing itself a collective of ecotypes. Ecologists adopt the distributed genome hypothesis of an open pan-genome to explain the observed genomic diversity and evolution patterns of the ecotypes within PC. Novel genomic data for the PC prompted us to revisit this group, applying the current methods used in genomic taxonomy. As a result, we were able to distinguish the five genera: Prochlorococcus, Eurycolium, Prolificoccus, Thaumococcus, and Riococcus. The novel genera have distinct genomic and ecological attributes. Keywords Prochlorococcus collective . Eco-genomics . Genomic taxonomy . Evolution

Introduction Prochlorococcus cells are the smallest cells that emit red chlorophyll fluorescence, which is how they were discovered approximately 30 years ago [1, 2]. It is the smallest and most abundant photosynthetic microbe on Earth. The oxytrophic free-living marine Prochlorococcus marinus contain divinyl chlorophyll a (chl a2) and both monovinyl and divinyl chlorophyll b (chl b2) as their major photosynthetic pigments rather than chlorophyll a and phycobiliproteins, which are typical of Cyanobacteria, allowing them to adapt to different light intensities [1, 3–6], particularly to capture the blue wavelengths prevailing in oligotrophic waters [7]. Prochlorococcus strains have been cultured and are available in culture collections, but the limited number of cultures does not reflect the true phenotypic and genomic Diogo Tschoeke and Vinicius W. Salazar contributed equally to this work. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01526-5) contains supplementary material, which is available to authorized users. * Cristiane Thompson [email protected] 1

Laboratory of Microbiology, SAGE-COPPE and Institute of Biology, Federal University of Rio de Janeiro, Av. Carlos Chagas Fo 373, Rio de Janeiro, RJ 21941-902, Brazil

2

Laboratory of Microbiology, Ghent University, Gent, Belgium

diversity found in the ocean [8]. Prochlorococcus is a smaller, differently pigmented variant of marine Synechococcus [2]. The pioneering work on the eco-genomics of Prochlorococcus was performed by Chisholm’s group at MIT [2, 9–15]. The taxonomy of the Prochlorococcus collective (PC) has been neglected in the last three decades. The designation PC was first coined by Kashtan et al. [11]. This collective comprises the genera Prochlorococcus, Prolificoccus,