Global Trends in Marine Plankton Diversity across Kingdoms of Life

Ibarbalz, Federico M.; Henry, Nicolas; Brandão, Manoela C.; Martini, Séverine; Busseni, Greta; Byrne, H. Michael; Coelho, Luís Pedro; Endo, Hisashi; Gasol, Josep M.; Gregory, Ann C.; Mahé, Frédéric; Rigonato, Janaína; Royo-Llonch, Marta; Salazar, Guillem; Sanz-Sáez, Isabel; Scalco, Eleonora; Soviadan, D.; Zayed, Ahmed A.; Zingone, Adriana; Labadie, Karine; Ferland, Joannie; Marec, Claudie; Picheral, Marc; Dimier, Céline; Poulain, Julie; Pisarev, Sergey; Carmichael, Margaux; Pelletier, Éric; Bopp, Laurent; Lombard, Fabien; Zinger, Lucie; Acinas, Silvia G.; Babin, Marcel; Bork, Peer; Boss, Emmanuel; Bowler, Chris; Cochrane, Guy; Vargas, Colomban de; Follows, Mick; Gorsky, Gabriel; Grimsley, Nigel; Guidi, Lionel; Hingamp, Pascal; Iudicone, Daniele; Jaillon, Olivier; Kandels, Stefanie; Karp‐Boss, Lee; Karsenti, Eric; Not, Fabrice; Ogata, Hiroyuki; Pesant, Stéphane; Poulton, Nicole; Raes, Jeroen; Sardet, Christian; Speich, Sabrina; Stemmann, Lars; Sullivan, Matthew B.; Sunagawa, Shinichi; Wincker, Patrick

doi:10.1016/j.cell.2019.10.008

Cited by 282 publications

(309 citation statements)

References 138 publications

(244 reference statements)

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“…Pelagic fauna typically display a latitudinal diversity gradient, with high species numbers in warm low-latitude waters and declining diversity toward higher latitudes [40]. Although a previous study of prokaryotes and eukaryotes using metabarcoding and image data showed no latitudinal diversity in the mesopelagic layer [29], our metabarcoding approach revealed clear latitudinal gradients of diversity in each layer and throughout the sampling layers. As shown by the diversity index and proportions of sequence reads, many phylogenetically-diverse species coexisted in oligotrophic warm waters at low latitudes, whereas fewer species dominated in the cold, food-rich waters at high latitudes, consistent with the estimates of global diversity of epipelagic copepods based on the morphological classifications [15, 41].…”

Section: Discussionmentioning

confidence: 88%

“…In addition to high taxonomic resolution, metabarcoding analysis provides nucleotide sequences of OTUs, which are expected to provide insights into large-scale evolutionary processes and the reasons underlying patterns of copepod diversity. The global patterns of community and diversity have been analyzed using metabarcoding analysis of 18S rRNA gene for eukaryotic organisms including copepods [3, 29]; however, large-scale Pacific regions have not been fully covered, and detailed mechanisms controlling community structure and diversity should be discussed using the metabarcoding approach for both epipelagic and mesopelagic copepods in the Pacific Ocean.…”

Section: Introductionmentioning

confidence: 99%

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Large-scale metabarcoding analysis of epipelagic and mesopelagic copepods in the Pacific

Hirai

Tachibana

Tsuda

2020

Preprint

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AbstractA clear insight into large-scale community structure of planktonic copepods is critical to understanding mechanisms controlling diversity and biogeography of marine taxa, owing to their high abundance, ubiquity, and sensitivity to environmental changes. Here, we applied a 28S metabarcoding approach to large-scale communities of epipelagic and mesopelagic copepods at 70 stations across the Pacific Ocean and three stations in the Arctic Ocean. Major patterns of community structure and diversity, influenced by water mass structures, agreed with results from previous morphology-based studies. However, large-scale metabarcoding approach could detected community changes even under stable environmental conditions, including changes in the north/south subtropical gyres and east/west areas within each subtropical gyre. There were strong effects of epipelagic environment on mesopelagic communities, and community subdivisions were observed in the environmentally-stable mesopelagic layer. In each sampling station, higher operational taxonomic unit (OTU) numbers and lower phylogenetic diversity were observed in the mesopelagic layer than in the epipelagic layer, indicating a recent rapid increase of species numbers in the mesopelagic layer. The phylogenetic analysis utilizing representative sequences of OTUs revealed trends of recent emergence of cold-water OTUs mainly distributed at high latitudes with low water temperatures. Conversely, high diversity of copepods at low latitudes was suggested to have been formed through long evolutionary history under high water temperature. The metabarcoding results suggest that evolutionary processes have strong impacts on current patterns of copepod diversity, and support the “out of the tropics” theory explaining latitudinal diversity gradients of copepods. Both diversity patterns in epipelagic and mesopelagic showed high correlations to sea surface temperature; thus, predicted global warming may have a significant impact on copepod diversity in both layers.Author SummaryMarine planktonic copepods are highly dominant and diverse, and revealing their community structure and diversity is important to understanding marine ecosystems. We used molecular-based metabarcoding to reveal a total of 205 copepod communities in the ‘sunlight’ or epipelagic layer (0– 200 m) and the ‘twilight’ or mesopelagic layer (200–500 m and 500–1,000 m), mainly in the Pacific Ocean (data for 70 stations), but also in the Arctic Ocean (data for three stations). Different copepod communities were found in each geographical region with different environmental conditions, including tropical, subtropical, transition, Kuroshio Current, California Current, subarctic and arctic areas. The metabarcoding method sensitively detected small changes of copepod community even in environmentally-stable subtropical ocean systems and the mesopelagic layer. A high diversity of copepods was detected at low latitudes, and copepod diversity was higher in the mesopelagic layer than in the epipelagic layer in each area. These diversity patterns were influenced by both evolutionary history and present environmental conditions. The copepod community in the mesopelagic layer was strongly influenced by environmental conditions in the epipelagic layer. Thus, predicted climate changes may affect marine ecosystems not only in the epipelagic layer but also in the mesopelagic layer.

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Section: Discussionmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Large-scale metabarcoding analysis of epipelagic and mesopelagic copepods in the Pacific

Hirai

Tachibana

Tsuda

2020

Preprint

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“…This is a three-fold difference compared to the 6.84% read recovery by the 892 MAGs generated in Delmont et al 2018 with Tara Oceans metagenomes (which excluded the Arctic sampling) 38 . Our high read recovery could be due to methodological variations (co-assembly and binning strategy, read mapping and filtering) but also to the lower diversity reported in polar prokaryotic communities, compared to those from the temperate ocean 40 .…”

Section: Co-assembly and Trends Of Prokaryotic Arctic Binsmentioning

confidence: 98%

“…This could be associated with genomes that have been vertically exported from the photic zone to the mesopelagic and/or transported by deep ocean currents to more temperate latitudes. Higher species richness of temperate mesopelagic waters compared to the Arctic could also affect this result 40 . Individual metatranscriptomic recruitments tend to be lower than metagenomic recruitments in temperate latitudes in all layers ( Figure S3), suggesting that even though the deep currents could connect polar prokaryotes, most cells probably remain in resting stages during transit through non-polar latitudes until reaching favorable habitats in the Southern Ocean 45 .…”

Section: Co-assembly and Trends Of Prokaryotic Arctic Binsmentioning

confidence: 99%

Ecogenomics of key prokaryotes in the arctic ocean

Royo-Llonch¹,

Sánchez²,

Ruiz‐González³

et al. 2020

Preprint

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The Arctic Ocean is a key player in the regulation of climate and at the same time is under increasing pressure as a result of climate change. Predicting the future of this ecosystem requires understanding of the responses of Arctic microorganisms to environmental change, as they are the main drivers of global biogeochemical cycles. However, little is known about the ecology and metabolic potential of active Arctic microbes. Here, we reconstructed a total of 3,550 metagenomic bins from 41 seawater metagenomes collected as part of the Tara Oceans expedition, covering five different Arctic Ocean regions as well as the sub-Arctic North Atlantic Ocean and including various depths and different seasons (spring to autumn). Of these bins, 530 could be classified as Metagenome Assembled Genomes (MAGs) and over 75% of them represented novel species. We describe their habitat range and environmental preferences, as well as their metabolic capabilities, building the most comprehensive dataset of uncultured bacterial and archaeal genomes from the Arctic Ocean to date. We found a prevalence of mixotrophs, while chemolithoautotrophs were mostly present in the mesopelagic Arctic Ocean during spring and autumn. Finally, the catalogue of Arctic MAGs was complemented with metagenomes and metatranscriptomes from the global ocean to identify the most active MAGs present exclusively in polar metagenomes. These polar MAGs, which display a range of metabolic strategies, might represent Arctic sentinels of climate change and should be considered in prospective studies of the future state of the Arctic Ocean.

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“…While the "paradox of the plankton" and its resolution based on the theory of chaos support the co-occurrence of functionally similar plankton (Huisman & Weissing, 1999;Hutchinson, 1961), here we show that indeed phylogenetic related plankton co-occur but could simultaneously co-exclude themselves more than expected by chance at the marine surface. Other large-scale processes affect the assembly patterns of marine sunlight exposure and currents responsible of the depth stratification in the water column (Giner et al, 2020;Ibarbalz et al, 2019). However, geographical structures, natural fluctuations and absence of equilibrium state in marine plankton communities are not enough to avoid exclusion among related organisms, as observed here, and would refute the existence of any plankton paradox under phylogenetic niche conservatism.…”

Section: Discussionmentioning

confidence: 73%

Relating network analyses to phylogenetic relatedness to infer protistan co-occurrences and co-exclusions in marine and terrestrial environments

Lentendu

Dunthorn

2020

Preprint

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We used two large-scale metabarcoding datasets to evaluate phylogenetic signals at global marine and regional terrestrial scales using co-occurrence and co-exclusion networks. Phylogenetic relatedness was estimated using either global pairwise sequence distance or phylogenetic distance and the significance of observed patterns relating networks and phylogenies were evaluated against two null models. In all datasets, we found that phylogenetically close OTUs significantly cooccurred more often, and OTUs with intermediate phylogenetic relatedness co-occurred less often, than expected by chance. Phylogenetically close OTUs co-excluded less often than expected by chance in the marine datasets only. Simultaneous excess of co-occurrences and co-exclusions were observed in the inversion zone between close and intermediate phylogenetic distance classes in marine surface. Similar patterns were observed by using either pairwise sequence or phylogenetic distances, and by using both null models. These results suggest that environmental filtering and dispersal limitation are the preponderant forces driving co-occurrence of protists in both environments, while signal of competitive exclusion was only detected in the marine surface environment. The discrepancy in the co-exclusion pattern is potentially linked to the individual 1 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 environments: water bodies are more homogeneous while tropical forest soils contain a myriad of nutrient rich micro-environment reducing the strength of mutual exclusion.

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Global Trends in Marine Plankton Diversity across Kingdoms of Life

Cited by 282 publications

References 138 publications

Large-scale metabarcoding analysis of epipelagic and mesopelagic copepods in the Pacific

Large-scale metabarcoding analysis of epipelagic and mesopelagic copepods in the Pacific

Ecogenomics of key prokaryotes in the arctic ocean

Relating network analyses to phylogenetic relatedness to infer protistan co-occurrences and co-exclusions in marine and terrestrial environments

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