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High temperature deep-sea vents support a rich phylogenetic and physiological diversity of thermophilic Bacteria and Archaea. The structure of the microbial communities associated with high temperature hydrothermal deposits (“chimneys”) is tightly coupled to the hydrothermal geochemistry and geographical location. From deep-sea hydrothermal samples that span the Pacific, Atlantic and Indian oceans, and collected between 1993-2018, we obtained 111 metagenomes to explore the temporal and spatial dynamics of the phylogenetic and functional diversity associated with high temperature chimneys. A total of 10,788 medium to high quality metagenome assembled genomes (MAGs) were obtained, with about 1938 archaeal and 8850 bacterial genomes. Our data represent a rich abundance of novel families, genera and species in the Archaea and Bacteria, providing much greater depth of genomic diversity of thermophiles from deep-sea vents. For example, within the Archaea alone, the Thermoprotei genomes are greatly expanded, and we obtained over 30 new MAGs associated with the Nanobdellales (Nanoarchaeota) that share many features of their cultivated relatives. Furthermore, within the marine thermophilic Bacteria, many groups that were previously not recognized to be globally significant in deep-sea high temperature ecosystems, such as the Minisyncoccota (previously CPR or Patecibacteria), can now be new targets for study and cultivation. We show that over time, the community structure in general is retained within sites, with examples of very closely related genomes being obtained over multiple years. While the hydrothermal geological setting and hence geochemistry does drive the microbial diversity, we show that functional redundancy ensures resilience and productivity in these ecosystems. 

ABSTRACT Aerobic anoxygenic phototrophic (AAP) bacteria harvest light energy using bacteriochlorophyll-containing reaction centers to supplement their mostly heterotrophic metabolism. While their abundance and growth have been intensively studied in coastal environments, much less is known about their activity in oligotrophic open ocean regions. Therefore, we combinedin situsampling in the North Pacific Subtropical Gyre, north of O'ahu island, Hawaii, with two manipulation experiments. Infra-red epifluorescence microscopy documented that AAP bacteria represented approximately 2% of total bacteria in the euphotic zone with the maximum abundance in the upper 50 m. They conducted active photosynthetic electron transport with maximum rates up to 50 electrons per reaction center per second. Thein situdecline of bacteriochlorophyll concentration over the daylight period, an estimate of loss rates due to predation, indicated that the AAP bacteria in the upper 50 m of the water column turned over at rates of 0.75–0.90 d⁻¹. This corresponded well with the specific growth rate determined in dilution experiments where AAP bacteria grew at a rate 1.05 ± 0.09 d⁻¹. An amendment of inorganic nitrogen to obtain N:P = 32 resulted in a more than 10 times increase in AAP abundance over 6 days. The presented data document that AAP bacteria are an active part of the bacterioplankton community in the oligotrophic North Pacific Subtropical Gyre and that their growth was mostly controlled by nitrogen availability and grazing pressure.IMPORTANCEMarine bacteria represent a complex assembly of species with different physiology, metabolism, and substrate preferences. We focus on a specific functional group of marine bacteria called aerobic anoxygenic phototrophs. These photoheterotrophic organisms require organic carbon substrates for growth, but they can also supplement their metabolic needs with light energy captured by bacteriochlorophyll. These bacteria have been intensively studied in coastal regions, but rather less is known about their distribution, growth, and mortality in the oligotrophic open ocean. Therefore, we conducted a suite of measurements in the North Pacific Subtropical Gyre to determine the distribution of these organisms in the water column and their growth and mortality rates. A nutrient amendment experiment showed that aerobic anoxygenic phototrophs were limited by inorganic nitrogen. Despite this, they grew more rapidly than average heterotrophic bacteria, but their growth was balanced by intense grazing pressure.