%0 Journal Article %J Environmental Microbiology %D 2023 %T The Bay of Bengal exposes abundant photosynthetic picoplankton and newfound diversity along salinity-driven gradients %A Strauss, Jan %A Choi, Chang Jae %A Grone, Jonathan %A Wittmers, Fabian %A Jimenez, Valeria %A Makareviciute-Fichtner, Kriste %A Bachy, Charles %A Jaeger, Gualtiero Spiro %A Poirier, Camille %A Eckmann, Charlotte %A Spezzano, Rachele %A Löscher, Carolin R. %A Sarma, V. V. S. S. %A Mahadevan, Amala %A Worden, Alexandra Z. %K RCC393 %K RCC809 %X The Bay of Bengal (BoB) is a 2,600,000 km2 expanse in the Indian Ocean upon which many humans rely. However, the primary producers underpinning food chains here remain poorly characterized. We examined phytoplankton abundance and diversity along strong BoB latitudinal and vertical salinity gradients-which have low temperature variation (27-29°C) between the surface and subsurface chlorophyll maximum (SCM). In surface waters, Prochlorococcus averaged 11.7 ± 4.4 × 104  cells ml-1 , predominantly HLII, whereas LLII and 'rare' ecotypes, HLVI and LLVII, dominated in the SCM. Synechococcus averaged 8.4 ± 2.3 × 104  cells ml-1 in the surface, declined rapidly with depth, and population structure of dominant Clade II differed between surface and SCM; Clade X was notable at both depths. Across all sites, Ostreococcus Clade OII dominated SCM eukaryotes whereas communities differentiated strongly moving from Arabian Sea-influenced high salinity (southerly; prasinophytes) to freshwater-influenced low salinity (northerly; stramenopiles, specifically, diatoms, pelagophytes, and dictyochophytes, plus the prasinophyte Micromonas) surface waters. Eukaryotic phytoplankton peaked in the south (1.9 × 104  cells ml-1 , surface) where a novel Ostreococcus was revealed, named here Ostreococcus bengalensis. We expose dominance of a single picoeukaryote and hitherto 'rare' picocyanobacteria at depth in this complex ecosystem where studies suggest picoplankton are replacing larger phytoplankton due to climate change. %B Environmental Microbiology %G eng %R 10.1111/1462-2920.16431 %0 Journal Article %J Communications Biology %D 2022 %T Genomic adaptation of the picoeukaryote Pelagomonas calceolata to iron-poor oceans revealed by a chromosome-scale genome sequence %A Guérin, Nina %A Ciccarella, Marta %A Flamant, Elisa %A Frémont, Paul %A Mangenot, Sophie %A Istace, Benjamin %A Noel, Benjamin %A Belser, Caroline %A Bertrand, Laurie %A Labadie, Karine %A Cruaud, Corinne %A Romac, Sarah %A Bachy, Charles %A Gachenot, Martin %A Pelletier, Eric %A Alberti, Adriana %A Jaillon, Olivier %A Wincker, Patrick %A Aury, Jean-Marc %A Carradec, Quentin %K Biogeography %K comparative genomics %K metagenomics %K RCC100 %K Water microbiology %X The smallest phytoplankton species are key actors in oceans biogeochemical cycling and their abundance and distribution are affected with global environmental changes. Among them, algae of the Pelagophyceae class encompass coastal species causative of harmful algal blooms while others are cosmopolitan and abundant. The lack of genomic reference in this lineage is a main limitation to study its ecological importance. Here, we analysed Pelagomonas calceolata relative abundance, ecological niche and potential for the adaptation in all oceans using a complete chromosome-scale assembled genome sequence. Our results show that P. calceolata is one of the most abundant eukaryotic species in the oceans with a relative abundance favoured by high temperature, low-light and iron-poor conditions. Climate change projections based on its relative abundance suggest an extension of the P. calceolata habitat toward the poles at the end of this century. Finally, we observed a specific gene repertoire and expression level variations potentially explaining its ecological success in low-iron and low-nitrate environments. Collectively, these findings reveal the ecological importance of P. calceolata and lay the foundation for a global scale analysis of the adaptation and acclimation strategies of this small phytoplankton in a changing environment. Genomic inference reveals potential climate change-driven range expansion of the phytoplankton species Pelagomonas calceolata. %B Communications Biology %V 5 %P 1–14 %G eng %U https://www.nature.com/articles/s42003-022-03939-z %R 10.1038/s42003-022-03939-z %0 Journal Article %J The ISME Journal %D 2021 %T Viruses infecting a warm water picoeukaryote shed light on spatial co-occurrence dynamics of marine viruses and their hosts %A Bachy, Charles %A Yung, Charmaine C. M. %A Needham, David M. %A Gazitúa, Maria Consuelo %A Roux, Simon %A Limardo, Alexander J. %A Choi, Chang Jae %A Jorgens, Danielle M. %A Sullivan, Matthew B. %A Worden, Alexandra Z. %K RCC715 %K RCC716 %X The marine picoeukaryote Bathycoccus prasinos has been considered a cosmopolitan alga, although recent studies indicate two ecotypes exist, Clade BI (B. prasinos) and Clade BII. Viruses that infect Bathycoccus Clade BI are known (BpVs), but not that infect BII. We isolated three dsDNA prasinoviruses from the Sargasso Sea against Clade BII isolate RCC716. The BII-Vs do not infect BI, and two (BII-V2 and BII-V3) have larger genomes (\textasciitilde210 kb) than BI-Viruses and BII-V1. BII-Vs share \textasciitilde90% of their proteins, and between 65% to 83% of their proteins with sequenced BpVs. Phylogenomic reconstructions and PolB analyses establish close-relatedness of BII-V2 and BII-V3, yet BII-V2 has 10-fold higher infectivity and induces greater mortality on host isolate RCC716. BII-V1 is more distant, has a shorter latent period, and infects both available BII isolates, RCC716 and RCC715, while BII-V2 and BII-V3 do not exhibit productive infection of the latter in our experiments. Global metagenome analyses show Clade BI and BII algal relative abundances correlate positively with their respective viruses. The distributions delineate BI/BpVs as occupying lower temperature mesotrophic and coastal systems, whereas BII/BII-Vs occupy warmer temperature, higher salinity ecosystems. Accordingly, with molecular diagnostic support, we name Clade BII Bathycoccus calidus sp. nov. and propose that molecular diversity within this new species likely connects to the differentiated host-virus dynamics observed in our time course experiments. Overall, the tightly linked biogeography of Bathycoccus host and virus clades observed herein supports species-level host specificity, with strain-level variations in infection parameters. %B The ISME Journal %P 1–19 %8 may %G eng %U https://www.nature.com/articles/s41396-021-00989-9 %R 10.1038/s41396-021-00989-9 %0 Journal Article %J Environmental Microbiology %D 2019 %T Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies %A Zimmerman, Amy E. %A Bachy, Charles %A Ma, Xiufeng %A Roux, Simon %A Jang, Ho Bin %A Sullivan, Matthew B. %A Waldbauer, Jacob R. %A Worden, Alexandra Z. %K rcc3401 %K RCC393 %K RCC829 %X SUMMARY In marine ecosystems viruses are major disrupters of the direct flow of carbon and nutrients to higher trophic levels. While the genetic diversity of several eukaryotic phytoplankton virus groups has been characterized, their infection dynamics are less understood, such that the physiological and ecological implications of their diversity remain unclear. We compared genomes and infection phenotypes of the two most closely related cultured phycodnaviruses infecting the widespread picoprasinophyte Ostreococcus lucimarinus under standard- (1.3 divisions d-1) and limited-light (0.41 divisions d-1) nutrient replete conditions. OlV7 infection caused early arrest of the host cell cycle, coinciding with a significantly higher proportion of infected cells than OlV1-amended treatments, regardless of host growth rate. OlV7 treatments showed a near-50-fold increase of progeny virions at the higher host growth rate, contrasting with OlV1's 16-fold increase. However, production of OlV7 virions was more sensitive than OlV1 production to reduced host growth rate, suggesting fitness trade-offs between infection efficiency and resilience to host physiology. Moreover, while organic matter released from OlV1- and OlV7-infected hosts had broadly similar chemical composition, some distinct molecular signatures were observed. Collectively, these results suggest that current views on viral relatedness through marker and core gene analyses underplay operational divergence and consequences for host ecology. This article is protected by copyright. All rights reserved. %B Environmental Microbiology %V 00 %G eng %R 10.1111/1462-2920.14608 %0 Journal Article %J The ISME Journal %D 2019 %T Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth %A Kashiyama, Yuichiro %A Yokoyama, Akiko %A Shiratori, Takashi %A Hess, Sebastian %A Not, Fabrice %A Bachy, Charles %A Gutierrez-Rodriguez, Andres %A Kawahara, Jun %A Suzaki, Toshinobu %A Nakazawa, Masami %A Ishikawa, Takahiro %A Maruyama, Moe %A Wang, Mengyun %A Chen, Man %A Gong, Yingchun %A Seto, Kensuke %A Kagami, Maiko %A Hamamoto, Yoko %A Honda, Daiske %A Umetani, Takahiro %A Shihongi, Akira %A Kayama, Motoki %A Matsuda, Toshiki %A Taira, Junya %A Yabuki, Akinori %A Tsuchiya, Masashi %A Hirakawa, Yoshihisa %A Kawaguchi, Akane %A Nomura, Mami %A Nakamura, Atsushi %A Namba, Noriaki %A Matsumoto, Mitsufumi %A Tanaka, Tsuyoshi %A Yoshino, Tomoko %A Higuchi, Rina %A Yamamoto, Akihiro %A Maruyama, Tadanobu %A Yamaguchi, Aika %A Uzuka, Akihiro %A Miyagishima, Shinya %A Tanifuji, Goro %A Kawachi, Masanobu %A Kinoshita, Yusuke %A Tamiaki, Hitoshi %K Biochemistry %K Biogeochemistry %K Cellular microbiology %K microbial ecology %K RCC164 %K RCC22 %K RCC24 %K RCC375 %K RCC916 %X Extant eukaryote ecology is primarily sustained by oxygenic photosynthesis, in which chlorophylls play essential roles. The exceptional photosensitivity of chlorophylls allows them to harvest solar energy for photosynthesis, but on the other hand, they also generate cytotoxic reactive oxygen species. A risk of such phototoxicity of the chlorophyll must become particularly prominent upon dynamic cellular interactions that potentially disrupt the mechanisms that are designed to quench photoexcited chlorophylls in the phototrophic cells. Extensive examination of a wide variety of phagotrophic, parasitic, and phototrophic microeukaryotes demonstrates that a catabolic process that converts chlorophylls into nonphotosensitive 132,173-cyclopheophorbide enols (CPEs) is phylogenetically ubiquitous among extant eukaryotes. The accumulation of CPEs is identified in phagotrophic algivores belonging to virtually all major eukaryotic assemblages with the exception of Archaeplastida, in which no algivorous species have been reported. In addition, accumulation of CPEs is revealed to be common among phototrophic microeukaryotes (i.e., microalgae) along with dismantling of their secondary chloroplasts. Thus, we infer that CPE-accumulating chlorophyll catabolism (CACC) primarily evolved among algivorous microeukaryotes to detoxify chlorophylls in an early stage of their evolution. Subsequently, it also underpinned photosynthetic endosymbiosis by securing close interactions with photosynthetic machinery containing abundant chlorophylls, which led to the acquisition of secondary chloroplasts. Our results strongly suggest that CACC, which allowed the consumption of oxygenic primary producers, ultimately permitted the successful radiation of the eukaryotes throughout and after the late Proterozoic global oxygenation. %B The ISME Journal %P 1 %8 feb %G eng %U http://www.nature.com/articles/s41396-019-0377-0 %R 10.1038/s41396-019-0377-0 %0 Journal Article %J Molecular biology and evolution %D 2015 %T Intron invasions trace algal speciation and reveal nearly identical Arctic and Antarctic Micromonas populations. %A Simmons, Melinda P %A Bachy, Charles %A Sudek, Sebastian %A van Baren, Marijke J %A Sudek, Lisa %A Ares, Manuel %A Worden, Alexandra Z %K rcc %X Spliceosomal introns are a hallmark of eukaryotic genes that are hypothesized to play important roles in genome evolution but have poorly understood origins. Although most introns lack sequence homology to each other, recently new families of spliceosomal introns that are repeated hundreds of times in individual genomes have been discovered in a few organisms. The prevalence and conservation of these introner elements (IEs) or introner-like elements (ILEs) in other taxa, as well as their evolutionary relationships to regular spliceosomal introns, are still unknown. Here, we systematically investigate introns in the widespread marine green alga Micromonas and report new families of IEs, numerous intron presence-absence polymorphisms, and potential intron insertion hot-spots. The new families enabled identification of conserved IE secondary structure features and establishment of a novel general model for repetitive intron proliferation across genomes. Despite shared secondary structure, the IE families from each Micromonas lineage bear no obvious sequence similarity to those in the other lineages, suggesting their appearance is intimately linked with the process of speciation. Two of the new IE families come from an Arctic culture (Micromonas Clade E2) isolated from a polar region where this alga is increasing in abundance due to climate change. The same two families were detected in metagenomic data from Antarctica - a system where Micromonas has never before been reported. Strikingly high identity between the Arctic isolate and Antarctic coding sequences that flank the IEs suggests connectivity between populations in the two polar systems that we postulate occurs through deep-sea currents. Recovery of Clade E2 sequences in North Atlantic Deep Waters beneath the Gulf Stream supports this hypothesis. Our work illuminates the dynamic relationships between an unusual class of repetitive introns, genome evolution, speciation and global distribution of this sentinel marine alga. %B Molecular biology and evolution %8 may %G eng %U http://mbe.oxfordjournals.org/cgi/content/long/msv122v1 %R 10.1093/molbev/msv122 %0 Journal Article %J Proceedings of the National Academy of Sciences of the United States of America %D 2014 %T Marine algae and land plants share conserved phytochrome signaling systems %A Duanmu, Deqiang %A Bachy, Charles %A Sudek, Sebastian %A Wong, Chee-Hong %A Jimenez, Valeria %A Rockwell, Nathan C %A Martin, Shelley S %A Ngan, Chew Yee %A Reistetter, Emily N %A van Baren, Marijke J %A Price, Dana C %A Wei, Chia-Lin %A Reyes-Prieto, Adrian %A Lagarias, J Clark %A Worden, Alexandra Z %K Micromonas %K rcc %X Phytochrome photosensors control a vast gene network in streptophyte plants, acting as master regulators of diverse growth and developmental processes throughout the life cycle. In contrast with their absence in known chlorophyte algal genomes and most sequenced prasinophyte algal genomes, a phytochrome is found in Micromonas pusilla, a widely distributed marine picoprasinophyte (¡2 µm cell diameter). Together with phytochromes identified from other prasinophyte lineages, we establish that prasinophyte and streptophyte phytochromes share core light-input and signaling-output domain architectures except for the loss of C-terminal response regulator receiver domains in the streptophyte phytochrome lineage. Phylogenetic reconstructions robustly support the presence of phytochrome in the common progenitor of green algae and land plants. These analyses reveal a monophyletic clade containing streptophyte, prasinophyte, cryptophyte, and glaucophyte phytochromes implying an origin in the eukaryotic ancestor of the Archaeplastida. Transcriptomic measurements reveal diurnal regulation of phytochrome and bilin chromophore biosynthetic genes in Micromonas. Expression of these genes precedes both light-mediated phytochrome redistribution from the cytoplasm to the nucleus and increased expression of photosynthesis-associated genes. Prasinophyte phytochromes perceive wavelengths of light transmitted farther through seawater than the red/far-red light sensed by land plant phytochromes. Prasinophyte phytochromes also retain light-regulated histidine kinase activity lost in the streptophyte phytochrome lineage. Our studies demonstrate that light-mediated nuclear translocation of phytochrome predates the emergence of land plants and likely represents a widespread signaling mechanism in unicellular algae. %B Proceedings of the National Academy of Sciences of the United States of America %V 111 %P 15827–15832 %G eng %U http://www.pnas.org/content/111/44/15827.abstract %R 10.1073/pnas.1416751111