Emerging concepts on microbial processes in the bathypelagic ocean – ecology, biogeochemistry, and genomics

Nagata, Toshi; Tamburini, Christian; Arı́stegui, Javier; Baltar, Federico; Bochdansky, Alexander B.; Fonda-Umani, S.; Fukuda, Hideki; Gogou, Alexandra; Hansell, Dennis A.; Hansman, Roberta L.; Herndl, Gerhard J.; Panagiotopoulos, Christos; Reinthaler, Thomas; Sohrin, Rumi; Verdugo, Pedro; Yamada, Namiha; Yamashita, Youhei; Yokokawa, Taichi; Bartlett, Douglas H.

doi:10.1016/j.dsr2.2010.02.019

Cited by 147 publications

(145 citation statements)

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“…Although the ALOHA 4000 m and PRT metagenomic analyses demonstrated subclade Ic organisms can be found in abysso-and hadopelagic realms, the lack of additional data from extreme deep water sites leaves the abundance of Pelagibacterales subclade Ic in such locations in question. Further, many previously identified features of both piezophilic isolates and deep ocean single-cell genomes (Simonato et al, 2006;Lauro and Bartlett, 2008;Nagata et al, 2010;Swan et al, 2011) are absent in the SAR11 SAGs. Although the incomplete state of the SAGs leaves open the possibility that these features may be contained in the unsequenced portion of the genomes, their absence in the nearly complete of AAA240-E13 SAG implies that even if present in some SAR11 Ic organisms, they are not universally conserved by the subclade.…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…The mesopelagic (200-1000 m) and bathypelagic (1000-4000 m) zones contain 470% of marine microbial biomass (Arıstegui et al, 2009) and these organisms have vital roles in global cycling of carbon, nitrogen and other biogeochemical processes (Nagata et al, 2010;Robinson et al, 2010). In addition to microorganisms necessarily being adapted to cold and increased pressure there, the deep sea also contains more recalcitrant forms of carbon than at the surface (Arıstegui et al, 2009;Nagata et al, 2010;Robinson et al, 2010). Cultivated isolates have revealed some microbial adaptations associated with life at depth, including increased intergenic spacer regions, rRNA gene indels and higher abundances of membrane polyunsaturated fatty acids and surface-adhesion/ motility genes (Simonato et al, 2006;Lauro and Bartlett, 2008;Wang et al, 2008;Nagata et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype

et al. 2014

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Bacterioplankton of the SAR11 clade are the most abundant microorganisms in marine systems, usually representing 25% or more of the total bacterial cells in seawater worldwide. SAR11 is divided into subclades with distinct spatiotemporal distributions (ecotypes), some of which appear to be specific to deep water. Here we examine the genomic basis for deep ocean distribution of one SAR11 bathytype (depth-specific ecotype), subclade Ic. Four single-cell Ic genomes, with estimated completeness of 55%-86%, were isolated from 770 m at station ALOHA and compared with eight SAR11 surface genomes and metagenomic datasets. Subclade Ic genomes dominated metagenomic fragment recruitment below the euphotic zone. They had similar COG distributions, high local synteny and shared a large number (69%) of orthologous clusters with SAR11 surface genomes, yet were distinct at the 16S rRNA gene and amino-acid level, and formed a separate, monophyletic group in phylogenetic trees. Subclade Ic genomes were enriched in genes associated with membrane/cell wall/envelope biosynthesis and showed evidence of unique phage defenses. The majority of subclade Ic-specfic genes were hypothetical, and some were highly abundant in deep ocean metagenomic data, potentially masking mechanisms for niche differentiation. However, the evidence suggests these organisms have a similar metabolism to their surface counterparts, and that subclade Ic adaptations to the deep ocean do not involve large variations in gene content, but rather more subtle differences previously observed deep ocean genomic data, like preferential amino-acid substitutions, larger coding regions among SAR11 clade orthologs, larger intergenic regions and larger estimated average genome size.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype

et al. 2014

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“…The physical conditions of this zone, in particular the low temperature ( À 1 1C to 3 1C), high pressure (10-50 MPa) and saturated oxygen concentrations, are globally quite stable, suggesting a seemingly homogeneous habitat. Nevertheless, even in this zone, it is possible to detect spatial gradients both for abiotic and biotic parameters caused by the different origins and properties of the bathypelagic water masses and by the inherent variability in the concentration and composition of organic constituents (Nagata et al, 2010). These gradients are expected to also influence the biologic realm.…”

Section: Introductionmentioning

confidence: 99%

“…The mesopelagic or twilight zone (200-1000 m), where the thermocline is often located, shows a great variability in water masses and associated physical parameters. This zone is considered to be crucial in organic matter remineralization, showing marked peaks or deficits of oxygen and inorganic nutrients (Nagata et al, 2010). Below, the bathypelagic zone (1000-4000 m) represents a much less variable environment.…”

Section: Introductionmentioning

confidence: 99%

Global abundance of planktonic heterotrophic protists in the deep ocean

et al. 2014

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The dark ocean is one of the largest biomes on Earth, with critical roles in organic matter remineralization and global carbon sequestration. Despite its recognized importance, little is known about some key microbial players, such as the community of heterotrophic protists (HP), which are likely the main consumers of prokaryotic biomass. To investigate this microbial component at a global scale, we determined their abundance and biomass in deepwater column samples from the Malaspina 2010 circumnavigation using a combination of epifluorescence microscopy and flow cytometry. HP were ubiquitously found at all depths investigated down to 4000 m. HP abundances decreased with depth, from an average of 72 ± 19 cells ml À 1 in mesopelagic waters down to 11 ± 1 cells ml À 1 in bathypelagic waters, whereas their total biomass decreased from 280±46 to 50±14 pg C ml À 1 . The parameters that better explained the variance of HP abundance were depth and prokaryote abundance, and to lesser extent oxygen concentration. The generally good correlation with prokaryotic abundance suggested active grazing of HP on prokaryotes. On a finer scale, the prokaryote:HP abundance ratio varied at a regional scale, and sites with the highest ratios exhibited a larger contribution of fungi molecular signal. Our study is a step forward towards determining the relationship between HP and their environment, unveiling their importance as players in the dark ocean's microbial food web.

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Impact of water mass mixing on the biogeochemistry and microbiology of the Northeast Atlantic Deep Water

Reinthaler

Salgado

Álvarez

et al. 2013

Global Biogeochemical Cycles

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[1] The extent to which water mass mixing contributes to the biological activity of the dark ocean is essentially unknown. Using a multiparameter water mass analysis, we examined the impact of water mass mixing on the nutrient distribution and microbial activity of the Northeast Atlantic Deep Water (NEADW) along an 8000 km long transect extending from 62°N to 5°S. Mixing of four water types (WT) and basin scale mineralization from the site where the WT where defined to the study area explained up to 95% of the variability in the distribution of inorganic nutrients and apparent oxygen utilization. Mixing-corrected average O 2 :N:P mineralization ratios of 127(±11):13.0(±0.7):1 in the core of the NEADW suggested preferential utilization of phosphorus compounds while dissolved organic carbon mineralization contributed a maximum of 20% to the oxygen demand of the NEADW. In conjunction with the calculated average mineralization ratios, our results indicate a major contribution of particulate organic matter to the biological activity in the NEADW. The variability in prokaryotic abundance, high nucleic acid containing cells, and prokaryotic heterotrophic production in the NEADW was explained by large scale (64-79%) and local mineralization processes (21-36%), consistent with the idea that deep-water prokaryotic communities are controlled by substrate supply. Overall, our results suggest a major impact of mixing on the distribution of inorganic nutrients and a weaker influence on the dissolved organic matter pool supporting prokaryotic activity in the NEADW.

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Emerging concepts on microbial processes in the bathypelagic ocean – ecology, biogeochemistry, and genomics

Cited by 147 publications

References 194 publications

Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype

Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype

Global abundance of planktonic heterotrophic protists in the deep ocean

Impact of water mass mixing on the biogeochemistry and microbiology of the Northeast Atlantic Deep Water

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