Global distribution, diversity, and ecological niche of Picozoa, a widespread and enigmatic marine protist lineage

Abstract

Background: The backbone of the eukaryotic tree of life contains taxa only found in molecular surveys, of which we still have a limited understanding. Such is the case of Picozoa, an enigmatic lineage of heterotrophic picoeukaryotes within the supergroup Archaeplastida, which has emerged as a significant component of marine microbial planktonic communities. To enhance our understanding of the diversity, distribution, and ecology of Picozoa, we conduct a comprehensive assessment at different levels, from assemblages to taxa, employing phylogenetic analysis, species distribution modeling, and ecological niche characterization.

Results: Picozoa was among the ten most abundant eukaryotic groups, found almost exclusively in marine environments. The phylum was represented by 179 Picozoa's OTU (pOTUs) placed in five phylogenetic clades. Picozoa community structure had a clear latitudinal pattern, with polar assemblages tending to cluster separately from non-polar ones. Based on the abundance and occupancy pattern, the pOTUs were classified into four categories: Low-abundant, Widespread, Polar, and Non-polar. We calculated the ecological niche of each of these categories. Notably, pOTUs sharing similar ecological niches were not closely related species, indicating a phylogenetic overdispersion in Picozoa communities. This could be attributed to competitive exclusion and the strong influence of the seasonal amplitude of variations in environmental factors, such as temperature, shaping physiological and ecological traits.

Conclusions: Overall, this work advances our understanding of uncharted protists' evolutionary dynamics and ecological strategies. Our results highlight the importance of understanding the species-level ecology of marine heteroflagellates like Picozoa. The observed phylogenetic overdispersion challenges the concept of phylogenetic niche conservatism in protist communities, suggesting that closely related species do not necessarily share similar ecological niches. Video Abstract.

Keywords: Ecological niche; Heterotrophic flagellates; Marine picoeukaryotic; Molecular diversity; Phylogenetic overdispersion; Picozoa; Protist; Species distribution modeling.

Fig. 1

Working hypotheses on the distribution and ecological niche of Picozoa. A Picozoa communities are latitudinally structured, with polar (tones of blue) assemblages clustering separately from non-polar ones (other colors). B Selection (or environmental filtering) is expected to play a larger role in this spatial distribution than species interactions, with temperature being one of the main drivers shaping the assemblage structure. C, D Consequently, Picozoa taxa sharing similar distribution patterns are likely to be phylogenetically related, indicating phylogenetic niche conservatism

Fig. 2

The spatial distribution of Picozoa. This figure shows the presence and absence of Picozoa sequences in different environments within the EukBank database, encompassing 12,570 georeferenced samples

Fig. 3

Maximum likelihood tree of Picozoa. A 18S rRNA reference tree constructed using 50 almost complete Picozoa sequences retrieved from the PR2 database (release v. 5.0.1). The tree was constructed in RAxML v.8.2.12 [53] with the GTRCATI model considering 1000 replicate trees for topology and 1000 trees for bootstrapping. Clades of Picozoa were based on this tree. B Phylogenetic representation of Picozoa and abundance distribution of clades across different oceans (AO Arctic Ocean, IO Indian Ocean, MS Mediterranean Sea, NAO North Atlantic Ocean, NPO North Pacific Ocean, SAO South Atlantic Ocean, SO Southern Ocean, SPO South Pacific Ocean) based on pOTU assignments (indicated in each clade)

Fig. 4

Picozoa community structure in the sunlit global ocean. A Sample ordination in a non-metric multidimensional scaling (NMDS) plot according to the similarity in Picozoa community structure (based on pOTUs relative abundance). Different oceans are indicated with color and latitudinal rank with symbols (AO Arctic Ocean, IO Indian Ocean, MS Mediterranean Sea, NAO North Atlantic Ocean, NPO North Pacific Ocean, SAO South Atlantic Ocean, SO Southern Ocean, SPO South Pacific Ocean). B Latitudinal variation of the Abundance, Richness, and Shannon–Weaver diversity index H′ of local Picozoa communities

Fig. 5

Latitudinal Distribution of Abundant pOTUs. This figure shows the habitat suitability index (HSI) of 53 abundant pOTUs for the global sunlit ocean, organized by their associated category based on the observed abundance and occupancy patterns (refer to Supplementary Fig. S6). Highest HSI index values indicate a higher probability of finding a pOTU in a given environment. Widespread pOTUs are indicated in green, Polar in blue, and Non-polar in red

Fig. 6

Ecological Niche and Niche Overlap of Abundant pOTUs. A Mean niche position of Polar (blue), Non-polar (red), and Widespread (green) pOTUs in the ecological space derived from the analyzed samples; grey dots represent the position of each sampling point in the ecological space. Arrowed lines depict canonical weightings of significant environmental factors contributing to the observed patterns. B Examples of estimated niche breadth using kernel density (colored lines represent 95% of probability distribution) in the environmental space for Widespread (green), Polar (blue), and Non-polar (red) pOTUs (refer to Supplementary Fig. S7); grey dots represent the position of each sampling point in the ecological space. C Schoener’s D index values representing niche overlap among pairs of abundant pOTUs. Highest Schoener’s D values indicate a higher niche overlap. Widespread pOTUs are indicated in green, Polar in blue, and Non-polar in red. Darker circles indicate higher overlap

Fig. 7

Phylogeny, Niche Similarity and Phylogenetic Overdispersion of Picozoa. 18S rRNA maximum likelihood circle tree (inverted) delineating Picozoa phylogenetic clades (refer to Fig. 3). The tree was constructed using reference sequences (highlighted in bold) and pOTUs considering 1000 replicates (refer to Fig. 3 and Supplementary Fig. S5). The colored circles inside indicate the category associated with each pOTU based on their abundance and occupancy pattern in the sunlit ocean (refer to Fig. 5 and Supplementary Fig. S6). Abundant pOTU are connected across the central circle by their niche overlap values, showing non-phylogenetic niche conservatism (only Schoener’s D values higher than 0.6 were considered, refer to Fig. 6). The colors of connecting lines indicate the niche overlap between pOTUs within the same clades (by corresponding color clades: strong pink for PIC-1A, soft green for PIC-1C, violet for PIC-2, greenish-brown for PIC-3, cyan for PIC-5) and from different clades (dark green)