Evolutionary pathways for deep-sea adaptation in marine planktonic Actinobacteriota
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The deep ocean, one of the largest ecosystems on earth, is dominated by microorganisms that are keystones in the regulation of biogeochemical cycles. However, the evolutionary pathways underlying the specific adaptations required (e.g., high pressure and low temperature) by this unique niche remain understudied. Here, we analyzed the first representatives belonging to the order Acidimicrobiales , a group of marine planktonic Actinobacteriota , that specifically inhabits the aphotic zone of the oceanic water column (>200 m). Compared with their epipelagic counterparts, deep-sea representatives showed the same evolution in genome architecture with higher GC content, longer intergenic spaces as well as higher nitrogen (N-ARSC) and lower carbon (C-ARSC) content in encoded amino acid residue side chains consistent with the higher nitrogen concentration and lower carbon concentration in deep waters compared to the photic zone. Metagenomic recruitment showed distribution patterns that allowed the description of different ecogenomic units within the three deep water-associated genera defined by our phylogenomic analyses (UBA3125, S20-B6 and UBA9410). The entire genus UBA3125 was found exclusively associated with oxygen minimum zones linked to the acquisition of genes involved in denitrification. Genomospecies of genus S20-B6 recruited in samples from both mesopelagic (200–1,000 m) and bathypelagic (1000–4,000 m) zones, including polar regions. Diversity in the genus UBA9410 was higher, with genomospecies widely distributed in temperate zones, others in polar regions, and the only genomospecies associated with abyssal zones (>4,000 m). At the functional level, groups beyond the epipelagic zone have a more complex transcriptional regulation including in their genomes a unique WhiB paralog. In addition, they showed higher metabolic potential for organic carbon and carbohydrate degradation as well as the ability to accumulate glycogen as a source of carbon and energy. This could compensate for energy metabolism in the absence of rhodopsins, which is only present in genomes associated with the photic zone. The abundance in deep samples of cytochrome P450 monooxygenases associated with the genomes of this order suggests an important role in remineralization of recalcitrant compounds throughout the water column.Keywords:
Mesopelagic zone
Bathyal zone
Oxygen minimum zone
Abstract. The faecal pellets (FPs) of zooplankton can be important vehicles for the transfer of particulate organic carbon (POC) to the deep ocean, often making large contributions to carbon sequestration. However, the routes by which these FPs reach the deep ocean have yet to be fully resolved. We address this by comparing estimates of copepod FP production to measurements of copepod FP size, shape, and number in the upper mesopelagic (175–205 m) using Marine Snow Catchers, and in the bathypelagic using sediment traps (1500–2000 m). The study is focussed on the Scotia Sea, which contains some of the most productive regions in the Southern Ocean, where epipelagic FP production is likely to be high. We found that, although the size distribution of the copepod community suggests that high numbers of small FPs are produced in the epipelagic, small FPs are rare in the deeper layers, implying that they are not transferred efficiently to depth. Consequently, small FPs make only a minor contribution to FP fluxes in the meso- and bathypelagic, particularly in terms of carbon. The dominant FPs in the upper mesopelagic were cylindrical and elliptical, while ovoid FPs were dominant in the bathypelagic. The change in FP morphology, as well as size distribution, points to the repacking of surface FPs in the mesopelagic and in situ production in the lower meso- and bathypelagic, which may be augmented by inputs of FPs via zooplankton vertical migrations. The flux of carbon to the deeper layers within the Southern Ocean is therefore strongly modulated by meso- and bathypelagic zooplankton, meaning that the community structure in these zones has a major impact on the efficiency of FP transfer to depth.
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Deep ocean microbial communities rely on the organic carbon produced in the sunlit ocean, yet it remains unknown whether surface processes determine the assembly and function of bathypelagic prokaryotes to a larger extent than deep-sea physicochemical conditions. Here, we explored whether variations in surface phytoplankton assemblages across Atlantic, Pacific and Indian ocean stations can explain structural changes in bathypelagic (ca. 4,000 m) free-living and particle-attached prokaryotic communities (characterized through 16S rRNA gene sequencing), as well as changes in prokaryotic activity and dissolved organic matter (DOM) quality. We show that the spatial structuring of prokaryotic communities in the bathypelagic strongly followed variations in the abundances of surface dinoflagellates and ciliates, as well as gradients in surface primary productivity, but were less influenced by bathypelagic physicochemical conditions. Amino acid-like DOM components in the bathypelagic reflected variations of those components in surface waters, and seemed to control bathypelagic prokaryotic activity. The imprint of surface conditions was more evident in bathypelagic than in shallower mesopelagic (200-1,000 m) communities, suggesting a direct connectivity through fast-sinking particles that escape mesopelagic transformations. Finally, we identified a pool of endemic deep-sea prokaryotic taxa (including potentially chemoautotrophic groups) that appear less connected to surface processes than those bathypelagic taxa with a widespread vertical distribution. Our results suggest that surface planktonic communities shape the spatial structure of the bathypelagic microbiome to a larger extent than the local physicochemical environment, likely through determining the nature of the sinking particles and the associated prokaryotes reaching bathypelagic waters.
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Abstract. The faecal pellets (FP) of zooplankton can be important vehicles for the transfer of particulate organic carbon (POC) to the deep ocean, often making large contributions to carbon sequestration. However, the routes by which these FP reach the deep ocean have yet to be fully resolved. We address this by comparing estimates of FP production to measurements of FP size, shape and number in the upper mesopelagic (175–205 m), using Marine Snow Catchers, and in the bathypelagic, using sediment traps (1,500–2,000 m). The study is focussed on the Scotia Sea, which contains some of the most productive regions in the Southern Ocean, where epipelagic FP production is likely to be high. We found that, although the size distribution of zooplankton suggests that high numbers of small FP are produced in the epipelagic, small FP are rare in the deeper layers, implying that they are not transferred efficiently to depth. Consequently, small FP make only a minor contribution to FP fluxes in the meso- and bathypelagic, particularly in terms of carbon. The dominant FP in the upper mesopelagic were cylindrical and elliptical, while ovoid FP were dominant in the bathypelagic. The change in FP morphology, as well as size distribution, points to the repacking of surface FP in the mesopelagic and in situ production in the lower meso- and bathypelagic, augmented by inputs of FP via zooplankton vertical migrations. The flux of carbon to the deeper layers within the Southern Ocean is therefore strongly modulated by meso- and bathypelagic zooplankton, meaning that the community structure in these zones has a major impact on the efficiency of FP transfer to depth.
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Data are reported from 30 dives during winter and spring 1980–83 at sites in the Strait of Georgia and inlets running off it, and in inlets on the west coast of Vancouver Island. Observations were made from the surface to the bottom (maximum 733 m) but most attention was given to the midwater plankton community. The vertical distribution and abundance of hydromedusae, siphonophores, ctenophores, euphausiids, pelagic worms and molluscs were recorded systematically, along with data for one copepod species ( Neocalanus plumchrus ). The midwater environment was found to be stable in terms of species composition and depth ranges, which permitted the data for several years and many locations to be pooled. Four categories of plankton are recognized: (a) epipelagic (concentrated in the top 50 m); (b) mesopelagic (50–175 m); (c) bathypelagic (below 175 m); and (d) meso-bathypelagic (forms living in both meso- and bathypelagic zones). Species in this last category behave like mesopelagic forms at the upper end of their ranges, migrating to the surface at night. Deeper-lying members of the same species do not migrate. For six such species, the cut-off point between migratory and non-migratory components was found to lie at a mean depth of 175 m. This depth is therefore taken as the demarcation point between the meso- and bathypelagic zones. Taking account of published data on light penetration, it is estimated that, for the whole region, daytime light intensity at 175 m, and hence the effective limit for phototaxis of the species in question, lies in the range 10 −8 –10 −9 μW cm −2 .
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The Earth’s most extensive living space is found in the bathypelagic zone of the oceans, yet research in these areas is scant. The micronekton of the bathypelagic zone in the eastern Gulf of Mexico (EGOM) was investigated with the goals of comparing its community structure and trophic interactions with those of the well-studied overlying mesopelagic micronekton. Significant changes in faunal structure were found, including shifts in dominant families as well as species. Compared to the mesopelagic zone, the bathypelagic community had increased abundance and biomass contributions from the Gonostomatidae, Oplophoridae, and Eucopiidae, with a simultaneous decrease in the importance of the Myctophidae and the Dendrobranchiata. The changed faunal structure within the crustacean assemblage includes a distinct difference in reproductive strategies. There is increased prevalence of taxa which feature egg brooding and abbreviated larval development. In addition, the bathypelagic zone was characterized by relatively large biomass contributions from rare but large species, particularly those within the families Oplophoridae and Nemichthyidae. The faunal shifts, in combination with a high percentage of bathypelagic species absent from mesopelagic samples (~50% of crustacean and ~37% of fish species), suggest the bathypelagic zone is home to a distinct pelagic community, with a biology and ecology fundamentally different from that of the mesopelagic zone. The broad zoogeographic distributions of bathypelagic species suggest the EGOM assemblage is possibly similar to that of other geographic locations at similar latitudes. Diet analysis was performed on several prominent species and revealed 2 major feeding strategies based on diet composition and prey size. Species of Cyclothone and Eucopia preyed
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The abundance and vertical distribution of micro-metazoans sampled with fine nets of 0.05 mm mesh size were studied at three stations in the Arabian Sea during the intermonsoon period (April/May 1987) and down to 1850 m depth. In the epipelagic zone (0–100 m). values of biomass and metazoan abundance tended to be higher than those reported for other tropical oceanic areas. In the mesopelagic zone, which is characterized by an extreme oxygen deficiency between 100 and 1000 m depth, the abundance of metazoan taxa and species numbers of non-calanoid copepods were largely reduced. However, intermediate abundance maxima occurred within this zone, which were dominated by specific metazoan taxa (copepods. appendicularians) and species of non-calanoids (Oncaea sp. C). In the bathypelagic zone below 1050 m, the species diversity of the dominant copepod family Oncaeidae increased substantially. Two-thirds of a total of 69 oncaeid species recovered were confined to this layer. As most of them were small in size and occurred in low abundance only, the increase in total oncaeid density and/or plankton biomass was less conspicuous. Dominant Oncaea species in the bathypelagic zone were O.longipes and O.brodskii. The results are compared with published data from the Arabian Sea and other tropical oceanic areas with and without an extreme mesopelagic oxygen minimum zone Possible causes of the intermediate abundance maxima within the oxygen deficiency zone are discussed.
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Abstract We assess the biomass of deep-pelagic shrimps in the Atlantic Ocean using data collected between 40°N and 40°S. Forty-eight stations were sampled in discrete-depth fashion, including epi- (0–200 m), meso- (200–800/1000 m), upper bathy- (800/1000–1500 m), and lower bathypelagic (1500–3000 m) strata. We compared samples collected from the same area on the same night using obliquely towed trawls and large vertically towed nets and found that shrimp catches from the latter were significantly higher. This suggests that vertical nets are more efficient for biomass assessments, and we report these values here. We further compared day and night samples from the same site and found that biomass estimates differed only in the epi- and mesopelagic strata, while estimates from the bathypelagic strata and the total water column were independent of time of day. Maximal shrimp standing stocks occurred in the upper bathypelagic (52–54% of total biomass) and in the mesopelagic (42–43%). We assessed shrimp biomass in three major regions of the Atlantic between 40°N and 40°S, and the first-order extrapolation of these data suggests that the global low-latitude deep-pelagic shrimp biomass (1700 million tons) may lie within the range reported for mesopelagic fishes (estimations between 1000 and 15000 million tons). These data, along with previous fish-biomass estimates, call for the reassessment of the quantity and distribution of nektonic carbon in the deep ocean.
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