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Phytoplankton community composition is a key determinant of ocean biogeochemical cycles, yet its observation from autonomous platforms remains challenging. In this study, we assessed the potential of in situ multispectral excitation fluorescence (MXF) to predict phytoplankton community structure indices in the Northwestern Mediterranean Sea. With a view toward applications on Biogeochemical-Argo (BGC-Argo) profiling floats, we evaluated a miniaturised, three-excitation-channel fluorometer. Laboratory measurements on ten phytoplankton strains confirmed that MXF ratios at 440, 470, and 532 nm provide taxon-specific signatures, especially for picocyanobacteria and green algae. Field observations of phytoplankton pigments were clustered into four ecologically distinct phytoplankton communities across the seasonal cycle, which defined the targeted phytoplankton community structure indices. A machine learning model was then trained to classify these clusters using MXF and additional bio-optical indices. Results show that existing BGC-Argo configurations (single-wavelength fluorescence, particulate backscattering, and beam attenuation coefficients) reliably distinguish broad community structures, such as pico- versus microphytoplankton dominance, but resolving finer pigment-based differences requires the additional spectral information provided by MXF. The different excitation channels contributed unequally: 440 and 470 nm provided robust pigment sensitivity across communities, while 532 nm was particularly informative for detecting phycoerythrin-rich taxa. Overall, combining MXF with bio-optical proxies improved classification performance by integrating pigment-specific and size-structure information, demonstrating the potential of MXF to enhance autonomous monitoring of phytoplankton community dynamics and their role in ocean biogeochemical cycles.

Marine Synechococcus cyanobacteria owe their ubiquity in part to the wide pigment diversity of their light-harvesting complexes. In open ocean waters, cells predominantly possess sophisticated antennae with rods composed of phycocyanin and two types of phycoerythrins (PEI and PEII). Some strains are specialized for harvesting either green or blue light, while others can dynamically modify their light absorption spectrum to match the dominant ambient color. This process, called type IV chromatic acclimation (CA4), has been linked to the presence of a small genomic island occurring in two configurations (CA4-A and CA4-B). While the CA4-A process has been partially characterized, the CA4-B process has remained an enigma. Here we characterize the function of two members of the phycobilin lyase E/F clan, MpeW and MpeQ, in Synechococcus sp. strain A15-62 and demonstrate their critical role in CA4-B. While MpeW, encoded in the CA4-B island and up-regulated in green light, attaches the green light-absorbing chromophore phycoerythrobilin to cysteine-83 of the PEII α-subunit in green light, MpeQ binds phycoerythrobilin and isomerizes it into the blue light-absorbing phycourobilin at the same site in blue light, reversing the relationship of MpeZ and MpeY in the CA4-A strain RS9916. Our data thus reveal key molecular differences between the two types of chromatic acclimaters, both highly abundant but occupying distinct complementary ecological niches in the ocean. They also support an evolutionary scenario whereby CA4-B island acquisition allowed former blue light specialists to become chromatic acclimaters, while former green light specialists would have acquired this capacity by gaining a CA4-A island.

Marine Synechococcus cyanobacteria owe their ubiquity in part to the wide pigment diversity of their lightharvesting complexes. In open ocean waters, cells predominantly possess sophisticated antennae with rods composed of phycocyanin and two types of phycoerythrins (PEI and PEII). Some strains are specialized for harvesting either green or blue light, while others can dynamically modify their light absorption spectrum to match the dominant ambient color. This process called 'Type-IV chromatic acclimation' (CA4) has been linked to the presence of a small genomic island occurring in two configurations (CA4-A and-B). While the CA4-A process has been partially characterized, the CA4-B process has remained an enigma. Here, we characterize the function of two members of the phycobilin lyase E/F clan, MpeW and MpeQ, in Synechococcus sp. strain A15-62 and demonstrate their critical role in CA4-B. While MpeW, encoded in the CA4-B island and upregulated in green light, attaches the green-light absorbing chromophore phycoerythrobilin to cysteine-83 of the PEII α-subunit in green light, MpeQ binds phycoerythrobilin and isomerizes it into the blue-light absorbing phycourobilin at the same site in blue light, reversing the relationship of MpeZ and MpeY in the CA4-A strain RS9916. Our data thus reveal key molecular differences between the two types of chromatic acclimaters, both highly abundant but occupying distinct complementary ecological niches in the ocean. They also support an evolutionary scenario whereby CA4-B island acquisition allowed former blue-light specialists to become chromatic acclimaters, while former green-light specialists would have acquired this capacity by gaining a CA4-A island. Significance Of all cyanobacteria on Earth, marine Synechococcus are those displaying the greatest pigment diversity. The most sophisticated pigment type are cells able to reversibly modify their color by a phenomenon called Type

Synechococcus is one of two most abundant phytoplanktonic organisms of the Ocean and also displays the widest variety of pigmentation of all marine oxyphotrophs, which makes it ideally suited to colonize the variety of spectral niches occurring in the upper-lit layer of oceans. Seven Synechococcus pigment types (PTs) have been described based on the composition and chromophorylation of their light-harvesting complexes, called phycobilisomes (PBS). The most sophisticated and abundant Synechococcus PT (3d) gathers cells capable of Type IV chromatic acclimation (CA4), i.e. to reversibly modify the ratio of the blue light-absorbing phycourobilin (PUB) to the green light-absorbing phycoerythrobilin (PEB) in PBS in order to match the ambient light color. Although two genetically distinct types of CA4-capable strains, so-called PTs 3dA and 3dB, have been evidenced and found to be equally abundant in the Ocean, reasons for their prevalence in natural Synechococcus populations remain obscure. Here, acclimation experiments in different blue to green ratios of representatives of these two PTs showed that in mixed blue-green light conditions, PT 3dB strains displayed significantly higher PUB:PEB ratios than their PT 3dA counterparts. Thus, PTs 3dA and 3dB seem to differ in the ratio of blue to green light required to trigger the CA4 process. Furthermore, shift experiments between 100% BL and 100% GL conditions, and conversely, also revealed discrepancies in the acclimation pace between the two types of chromatic acclimaters, which may explain their co-occurrence in some blue green light niches.

Competition between phytoplankton species for light has triggered an extensive diversification of photosynthetic pigments. In Synechococcus cyanobacteria, three major pigment types occur in the ocean: blue light (BL) specialists that have a high ratio of the BL-absorbing chromophore phycourobilin (PUB) to the green light (GL)-absorbing chromophore phycoerythrobilin (PEB), GL specialists that have a low PUB:PEB ratio, and cells that modify their PUB:PEB ratio to match the ambient color, a process called ‘Type IV chromatic acclimation’ (CA4). The abundance of CA4-capable cells in marine ecosystems suggests that CA4 confers a fitness advantage in certain light conditions compared to cells with fixed pigmentation. This hypothesis was tested by performing mono- and co-cultures of a BL specialist, a GL specialist and a CA4-capable strain in chemostats under different light conditions. Monocultures enabled us to parameterize a resource competition model that was used to predict competition between the three pigment types in co-cultures. In line with the model predictions, the BL specialist won in low blue light and the GL specialist won in low and high green light. Interestingly, we found that while the CA4-capable strain was at a disadvantage at low light, it was able to outcompete specialists in high blue light.

Marine Synechococcus cyanobacteria are ubiquitous in the ocean, a feature likely related to their extensive genetic diversity. Amongst the major lineages, clades I and IV preferentially thrive in temperate and cold, nutrient-rich waters, whilst clades II and III prefer warm, nitrogen or phosphorus-depleted waters. The existence of such cold (I/IV) and warm (II/III) thermotypes is corroborated by physiological characterization of representative strains. A fifth clade, CRD1, was recently shown to dominate the Synechococcus community in iron-depleted areas of the world ocean and to encompass three distinct ecologically significant taxonomic units (ESTUs CRD1A-C) occupying different thermal niches, suggesting that distinct thermotypes could also occur within this clade. Here, using comparative thermophysiology of strains representative of these three CRD1 ESTUs we show that the CRD1A strain MITS9220 is a warm thermotype, the CRD1B strain BIOS-U3-1 a cold temperate thermotype, and the CRD1C strain BIOS-E4-1 a warm temperate stenotherm. Curiously, the CRD1B thermotype lacks traits and/or genomic features typical of cold thermotypes. In contrast, we found specific physiological traits of the CRD1 strains compared to their clade I, II, III and IV counterparts, including a lower growth rate and photosystem II maximal quantum yield at most temperatures and a higher turnover rate of the D1 protein. Together, our data suggests that the CRD1 clade prioritizes adaptation to low-iron conditions over temperature adaptation, even though the occurrence of several CRD1 thermotypes likely explains why the CRD1 clade as a whole occupies most iron-limited waters. Competing Interest Statement The authors have declared no competing interest.