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The widespread distribution of Prochlorococcus can be attributed to the extensive genetic diversity that allows them to adapt to various oligotrophic environments. We investigated the adaptation of Prochlorococcus to nutrient environments in the surface eastern Indian Ocean (EIO, 16.5°N to 20°S, 88°E) in November 2018. The growth rate of the Prochlorococcus population and its response to macronutrient enrichments (NH4+andPO43− ${{\text{NH}}_{4}}^{+}\,\text{and}\,{{\text{PO}}_{4}}^{3-}$) and the abundance of functional gene modules related to nutrient utilization were examined by on‐deck incubation experiments and metagenomic analysis, respectively. Although the dissolved inorganic nitrogen was depleted (∼58 nM) and the Prochlorococcus populations were dominated by the high‐light‐adapted II ecotype, Prochlorococcus populations showed distinct physiological patterns, especially the response to macronutrient enrichments, indicating their adaptation to local nutrient environments. At the northernmost station in the Bay of Bengal, the significant increase in growth rate with macronutrient enrichments and the highest abundance of the phosphate starvation response two‐component regulatory system module indicated adaptation to phosphorus‐limited environments. In the southern EIO, the insignificant increase in growth rate with macronutrient enrichment and higher abundance of the iron complex transport system module suggested adaptation to iron‐limited environments. However, genomic characteristics are not always associated with physiological characteristics. The abundance of the nitrate/nitrite transport system module was higher in the southern EIO, where the growth of Prochlorococcus relied on regenerated nitrogen sources as revealed by incubation experiments. These results reflected the complexity of Prochlorococcus adaptation especially in chronically oligotrophic environments, which was better revealed by combining physiological and genomic analyses. Plain Language Summary: Prochlorococcus are the smallest but most abundant photosynthetic organisms on Earth. Their widespread distribution (40°N to 40°S) and dominance in global subtropical and tropical phytoplankton communities could be attributed to the extensive genetic diversity that allows them to adapt to various environments. Although the adaptation of Prochlorococcus to nutrient environments could be reflected by variation in the genome, this method sometimes masks the complexity of Prochlorococcus adaptation. In this study, we combined incubation experiments with metagenomic analysis to better understand Prochlorococcus adaptation in the eastern Indian Ocean, which is consistently nutrient‐depleted but has subtle variations in nutrient environments. The results showed that the Prochlorococcus population had three distinct physiological patterns in the study area. In particular, the distinct response to the additional nutrients in incubation experiments indicated their specific adaptations to local nutrient environments. Furthermore, by considering the physiological characteristics with the spatially varied abundance of functional genes related to nutrient acquisition, it was revealed that Prochlorococcus growth was limited by different nutrients (nitrogen, phosphorus or iron) across the study area. Our results suggested the complexity of Prochlorococcus adaptation to oligotrophic environments, which can be elucidated by considering both physiological and genomic characteristics. Key Points: Prochlorococcus had varied physiological and genomic characteristics as adaptations to nutrient environments in the eastern Indian OceanProchlorococcus adapted to phosphorus‐ and iron‐limited environments in the Bay of Bengal and southern eastern Indian Ocean, respectivelyThe adaptation of Prochlorococcus could be complex and better revealed by conducting both the physiological and genomic analyses [ABSTRACT FROM AUTHOR]

Picophytoplankton (pico) in the eastern Indian Ocean (EIO) were investigated during the inter-monsoon periods. They were found to typically comprise Prochlorococcus (Pro), Synechococcus (Syn), and Picoeukaryotes (PEuks). In the survey area, the pico showed two different vertical distribution patterns in different regions, whereby the Syn abundance decreased with depth, whereas those of Pro and PEuks increased and then decreased with depth, with the maximum depths ranging from 50 to 100 m. The cell abundance and community structure of the pico were similar at the equator (EQ) and the eastern boundary of the Indian Ocean near Sumatra (EB), but the pico cell abundance was significantly lower in the Bay of Bengal (BOB). Pro dominated most regions of the entire EIO and were approximately one-to-two orders of magnitude more abundant than Syn and PEuks. The distributions of Syn and PEuks showed little difference across various regions. Influenced by the physicochemistry of circulation and water masses, there were many different environmental factors in the different regions. The abundance of pico domination by Pro showed a strong positive correlation with the nutrients and salinity in the survey area, indicating increasing nutrient availability, particularly in the oligotrophic EIO. Generalized additive models (GAMs) analysis showed the differences in their responses to environmental variability. Pro and PEuks both increased strongly with warming up to below 26 °C, and Pro and PEuks were more responsive to chemical (nutrient) variability. Syn showed a broader tolerance of low-salinity conditions. In a certain range, an increase in nitrite and nitric acid can improve the cell abundance of Pro. As a significant contributor to primary productivity in oligotrophic waters, this study provides essential information for studying pico communities in the EIO and its adjacent marine ecosystems. [ABSTRACT FROM AUTHOR]

The present study involves the first measurements of size-fractionated biogenic silica (bSi) standing stocks and production rates in the oligotrophic Eastern Indian Ocean. The 150-m integrated bSi standing stocks in the pico- and nanosized fractions averaged 49% and 39%, respectively, of the total; the contributions of pico- and nanoplankton to total bSi production rates were 43% and 38%, respectively, together suggesting that these smaller plankton contributed a significant proportion of both the total bSi standing stock and its rate of production. The total bSi variability appeared to be driven by smaller-plankton dynamics. Also, our results suggest that the detrital bSi stocks were potentially sustained by the pico- and nanosized siliceous organisms (for example, Minidiscus and Synechococcus) instead of broken fragments of large diatoms or other siliceous microplankton. In particular, the atomically dense structure from Synechococcus cell lysis was enriched in Si element compared with intact cells. The factors controlling size-fractionated bSi standing stocks may be biological rather than physical processes, and the clear correlation between picoeukaryotes and the < 2 μm bSi further confirmed the possibility of Si accumulation by other smaller plankton. [ABSTRACT FROM AUTHOR]

Currently, there is scant information about the biodiversity and functional diversity of microbes in the eastern Indian Ocean (EIO). Here, we used a combination of high-throughput sequencing of 16S rRNA genes and a metagenomic approach to investigate the microbial population structure and its metabolic function in the equatorial EIO. Our results show that Cyanobacterial Prochlorococcus made up the majority of the population. Interestingly, there were fewer contributions from clades SAR11 (Alphaproteobacteria) and SAR86 (Gammaproteobacteria) to microbial communities than contributions from Prochlorococcus. Based on functional gene analysis, functional genes rbcL, narB, and nasA were relatively abundant among the relevant genes. The abundance of Prochlorococcus implies its typically ecological adaptation in the local ecosystem. The microbial metabolic potential shows that in addition to the main carbon fixation pathway Calvin cycle, the rTCA cycle and the 3-HP/4-HB cycle have potential alternative carbon fixation contributions to local ecosystems. For the nitrogen cycle, the assimilatory nitrate and nitrite reduction pathway is potentially the crucial form of nitrogen utilization; unexpectedly, nitrogen fixation activity was relatively weak. This study extends our knowledge of the roles of microbes in energy and resource cycling in the EIO and provides a foundation for revealing profound biogeochemical processes driven by the microbial community in the ocean.

Photosynthesis by picophytoplankton provides energy for higher organisms and is essential in the food chain and global carbon cycle. In 2020 and 2021, we investigated the spatial distribution and vertical changes of picophytoplankton in the euphotic layer of the Eastern Indian Ocean (EIO) and estimated their carbon biomass contributions through two cruise surveys. The abundance of picophytoplankton was composed of Prochlorococcus (69.94%), Synechococcus (22.21%) and picoeukaryotes (7.85%). Synechococcus was mainly found in the surface layer, while Prochlorococcus and picoeukaryotes had high abundances in the subsurface layer. The surface picophytoplankton community was greatly affected by fluorescence, the middle layer was significantly regulated by temperature and dissolved oxygen concentration, and the lower layer was dominated by nutrients and apparent oxygen utilization (AOU). Aggregated boosted tree (ABT) and Generalized Additive models (GAM) indicated that temperature, salinity, AOU, and fluorescence were strong influencing factors of picophytoplankton communities in EIO. The mean carbon biomass contribution of picophytoplankton in the surveyed area was 0.565 μg C/L, which was contributed by Prochlorococcus (39.32%), Synechococcus (38.88%) and picoeukaryotes (21.80%). These findings contribute to our understanding of the effects of different environmental factors on picophytoplankton communities and the influence of picophytoplankton contributions to the carbon pools of the oligotrophic ocean. • The distribution and composition of picophytoplankton are characterized by strong spatial and vertical variation. • The relationship between picophytoplankton and environmental factors was analyzed using ABT and GAMs models. • The carbon biomass contribution of picophytoplankton is determined by both abundance and volume. • Temperature, fluorescence and oxygen are key environmental factors affecting picophytoplankton in the Eastern Indian Ocean. [ABSTRACT FROM AUTHOR]

Simple Summary: Marine microbes are regarded as the most diverse organisms in the biosphere and drive biogeochemical cycles through their metabolism. It is essential to understand the structure and metabolic function of microbial communities. The Indian Ocean is the third largest ocean in the world, and it possesses unique hydrographical properties. So far, assessments of microbial diversity and metabolism need to be improved in the Indian Ocean. Therefore, we carried out a series of investigations in the equatorial eastern Indian Ocean in order to clarify the local microbial communities and detect the genetic potential for microbial functions. The obtained results suggested Cyanobacteria was the dominant microbial group, and predicted the Calvin cycle and the assimilatory nitrate and nitrite reduction played important role in the pathway of carbon fixation and nitrogen metabolism respectively. This study provides insights into microbial community structures as well as the metabolic potential that may be active in the local environment, and lays the groundwork for understanding the roles of microbes in energy and resource cycling in this habitat. Currently, there is scant information about the biodiversity and functional diversity of microbes in the eastern Indian Ocean (EIO). Here, we used a combination of high-throughput sequencing of 16S rRNA genes and a metagenomic approach to investigate the microbial population structure and its metabolic function in the equatorial EIO. Our results show that Cyanobacterial Prochlorococcus made up the majority of the population. Interestingly, there were fewer contributions from clades SAR11 (Alphaproteobacteria) and SAR86 (Gammaproteobacteria) to microbial communities than contributions from Prochlorococcus. Based on functional gene analysis, functional genes rbcL, narB, and nasA were relatively abundant among the relevant genes. The abundance of Prochlorococcus implies its typically ecological adaptation in the local ecosystem. The microbial metabolic potential shows that in addition to the main carbon fixation pathway Calvin cycle, the rTCA cycle and the 3-HP/4-HB cycle have potential alternative carbon fixation contributions to local ecosystems. For the nitrogen cycle, the assimilatory nitrate and nitrite reduction pathway is potentially the crucial form of nitrogen utilization; unexpectedly, nitrogen fixation activity was relatively weak. This study extends our knowledge of the roles of microbes in energy and resource cycling in the EIO and provides a foundation for revealing profound biogeochemical processes driven by the microbial community in the ocean. [ABSTRACT FROM AUTHOR]