Evolutionary diversification of tiny ocean predators

Latorre, Francisco; Deutschmann, Ina Maria; Labarre, Aurélie; Obiol,; Krabberod,; Pelletier,; Sieracki, Michael E.; Cruaud,; Jaillon, Olivier; Massana, Ramón; Logares,

doi:10.1101/2020.10.09.333062

Cited by 3 publications

(3 citation statements)

References 95 publications

(90 reference statements)

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“…Coassembled genome completeness was estimated with BUSCO v3. For each coassembly, protein-coding genes were predicted de novo with AUGUSTUS 3.2.3 (87, 88) using the identified BUSCO v3 proteins as training set (89). Predicted genes were functionally annotated using 1) CAZy database from dbCAN v6 (90) and HMMER 3.1b2 (91), 2) KEGG [Release 2015-10-12; (92, 93)], and 3) eggNOG v4.5 (94), both using BLAST 2.2.28+.…”

Section: Methodsmentioning

confidence: 99%

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Niche adaptation promoted the evolutionary diversification of tiny ocean predators

Latorre

Deutschmann

Labarre

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Unicellular eukaryotic predators play a crucial role in the functioning of the ocean ecosystem by recycling nutrients and energy that are channeled to upper trophic levels. Traditionally, these evolutionarily diverse organisms have been combined into a single functional group (heterotrophic flagellates), overlooking their organismal differences. Here, we investigated four evolutionarily related species belonging to one cosmopolitan group of uncultured marine picoeukaryotic predators: marine stramenopiles (MAST)-4 (species A, B, C, and E). Co-occurrence and distribution analyses in the global surface ocean indicated contrasting patterns in MAST-4A and C, suggesting adaptation to different temperatures. We then investigated whether these spatial distribution patterns were mirrored by MAST-4 genomic content using single-cell genomics. Analyses of 69 single cells recovered 66 to 83% of the MAST-4A/B/C/E genomes, which displayed substantial interspecies divergence. MAST-4 genomes were similar in terms of broad gene functional categories, but they differed in enzymes of ecological relevance, such as glycoside hydrolases (GHs), which are part of the food degradation machinery in MAST-4. Interestingly, MAST-4 species featuring a similar GH composition (A and C) coexcluded each other in the surface global ocean, while species with a different set of GHs (B and C) appeared to be able to coexist, suggesting further niche diversification associated with prey digestion. We propose that differential niche adaptation to temperature and prey type has promoted adaptive evolutionary diversification in MAST-4. We show that minute ocean predators from the same phylogenetic group may have different biogeography and genomic content, which needs to be accounted for to better comprehend marine food webs.

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Section: Methodsmentioning

confidence: 99%

“…Genome coassemblies, coding sequence predictions, and amino acid predictions have been deposited in FigShare (DOI: 10.6084/m9.figshare. 13072322) (89). All other study data are included in the article and/or supporting information.…”

Section: Methodsmentioning

confidence: 99%

Niche adaptation promoted the evolutionary diversification of tiny ocean predators

Latorre

Deutschmann

Labarre

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Thus, if the study aim is to explore patterns of network topology 466 rather than single edges, inferring a network comparable to the real interaction network may be more useful than accuracy of single edges. However, investigations aiming to provide potential interaction partners may use EnDED with the intersection combination approach 469 (e.g., (Latorre et al, 2021)). Specific associations may be validated with experiments or microscopy (Lima-Mendez et al, 2015;Krabberød et al, 2017).…”

Section: Future Perspectives 460mentioning

confidence: 99%

Disentangling environmental effects in microbial association networks

Deutschmann

Lima‐Mendez

Krabberød

et al. 2021

Preprint

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Background Ecological interactions among microorganisms are fundamental for ecosystem function, yet they are mostly unknown or poorly understood. High-throughput-omics can indicate microbial interactions through associations across time and space, which can be represented as association networks. Associations could result from either ecological interactions between microorganisms, or from environmental selection, where the associations are environmentally-driven. Therefore, before downstream analysis and interpretation, we need to distinguish the nature of the association, particularly if it is due to environmental selection or not. Results We present EnDED (Environmentally-Driven Edge Detection), an implementation of four approaches as well as their combination to predict which links between microorganisms in an association network are environmentally-driven. The four approaches are Sign Pattern, Overlap, Interaction Information, and Data Processing Inequality. We tested EnDED on networks from simulated data of 50 microorganisms. The networks contained on average 50 nodes and 1087 edges, of which 60 were true interactions but 1026 false associations (i.e. environmentally-driven or due to chance). Applying each method individually, we detected a moderate to high number of environmentally-driven edges - 87% Sign Pattern and Overlap, 67% Interaction Information, and 44% Data Processing Inequality. Combining these methods in an intersection approach resulted in retaining more interactions, both true and false (32% of environmentally-driven associations). After validation with the simulated datasets, we applied EnDED on a marine microbial network inferred from 10 years of monthly observations of microbial-plankton abundance. The intersection combination predicted that 8.3% of the associations were environmentally-driven, while individual methods predicted 24.8% (Data Processing Inequality), 25.7% (Interaction Information), and up to 84.6% (Sign Pattern as well as Overlap). The fraction of environmentally-driven edges among negative microbial associations in the real network increased rapidly with the number of environmental factors. Conclusions To reach accurate hypotheses about ecological interactions, it is important to determine, quantify, and remove environmentally-driven associations in marine microbial association networks. For that, EnDED offers up to four individual methods as well as their combination. However, especially for the intersection combination, we suggest using EnDED with other strategies to reduce the number of false associations and consequently the number of potential interaction hypotheses.

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Comparative genomics reveals new functional insights in uncultured MAST species

et al. 2021

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Heterotrophic lineages of stramenopiles exhibit enormous diversity in morphology, lifestyle, and habitat. Among them, the marine stramenopiles (MASTs) represent numerous independent lineages that are only known from environmental sequences retrieved from marine samples. The core energy metabolism characterizing these unicellular eukaryotes is poorly understood. Here, we used single-cell genomics to retrieve, annotate, and compare the genomes of 15 MAST species, obtained by coassembling sequences from 140 individual cells sampled from the marine surface plankton. Functional annotations from their gene repertoires are compatible with all of them being phagocytotic. The unique presence of rhodopsin genes in MAST species, together with their widespread expression in oceanic waters, supports the idea that MASTs may be capable of using sunlight to thrive in the photic ocean. Additional subsets of genes used in phagocytosis, such as proton pumps for vacuole acidification and peptidases for prey digestion, did not reveal particular trends in MAST genomes as compared with nonphagocytotic stramenopiles, except a larger presence and diversity of V-PPase genes. Our analysis reflects the complexity of phagocytosis machinery in microbial eukaryotes, which contrasts with the well-defined set of genes for photosynthesis. These new genomic data provide the essential framework to study ecophysiology of uncultured species and to gain better understanding of the function of rhodopsins and related carotenoids in stramenopiles.

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Evolutionary diversification of tiny ocean predators

Cited by 3 publications

References 95 publications

Niche adaptation promoted the evolutionary diversification of tiny ocean predators

Niche adaptation promoted the evolutionary diversification of tiny ocean predators

Disentangling environmental effects in microbial association networks

Comparative genomics reveals new functional insights in uncultured MAST species

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