Insight into planktonic protistan and fungal communities across the nutrient-depleted environment of the South Pacific Subtropical Gyre

Abstract

Ocean microorganisms constitute ~70% of the marine biomass, contribute to ~50% of the Earth's primary production, and play a vital role in global biogeochemical cycles. The marine heterotrophic and mixotrophic protistan and fungal communities have often been overlooked mainly due to limitations in morphological species identification. Despite the accumulation of studies on biogeographic patterns observed in microbial communities, our understanding of the abundance and distribution patterns within the microbial community of the largest subtropical gyre, the South Pacific Gyre (SPG), remains incomplete. Here, we investigated the diversity and vertical composition of protistan and fungal communities in the water column of the ultra-oligotrophic SPG. Our results showed apparent differences in protistan community diversity in the photic and aphotic regions. The entire protistan community diversity was significantly affected by temperature, salinity, oxygen, and nutrient concentrations, while the parasitic community diversity was also affected by chlorophyll a concentration. The parasitic protists were assigned to the class Syndiniales accounting for over 98% of the total parasitic protists, exhibiting higher relative sequence abundance along the water depth and displaying consistent patterns among different sampling stations. In contrast to the protistan community, the fungal community along the SPG primarily clustered based on the sampling station and pelagic zones. In particular, our study reveals a significant presence of parasitic protists and functionally diverse fungi in SPG and their potential impact on carbon cycling in the gyre.IMPORTANCEOur findings carry important implications for understanding the distribution patterns of the previously unrecognized occurrence of parasitic protists and functionally diverse fungi in the nutrient-limited South Pacific Gyre. In particular, our study reveals a significant presence of parasitic Syndiniales, predominantly abundant in the upper 300 m of the aphotic zone in the gyre, and a distinct presence of fungal communities in the aphotic zone at the central part of the gyre. These findings strongly suggest that these communities play a substantial role in yet insufficiently described microbial food web. Moreover, our research enhances our understanding of their contribution to the dynamics of the food webs in oligotrophic gyres and is valuable for projecting the ecological consequences of future climate warming.

Keywords: South Pacific Subtropical Gyre; fungi; parasitic protists.

Fig 1

Map of sampling stations along the SO245 UltraPac transect. Black points denote sampling stations; samples used in the following study were collected at the enumerated dots. Gray arrows show the main ocean currents. The map was made in R and finished in Inkscape.

Fig 2

Partitioning of protistan major taxonomic groups by irradiance zone in South Pacific Gyre. Heatmap of relative sequence abundance of protistan community at the order level (orders with relative sequence abundance > 1%). Columns were clustered based on Bray-Curtis distance with the top row colored by irradiance zone. Abundances were log-transformed. Below the heatmap, the plot shows the relative sequence abundance of parasitic protists in clustered samples.

Fig 3

Vertical differences in the protistan community in South Pacific Gyre. (A) Number of unique, shared, and ubiquitous ASVs of all protists and parasitic protists across the photic and aphotic zones. Color-coded categories by irradiance zone (photic and aphotic zone). (B) Principal coordinate analysis (PCoA) of protistan community diversity color coded by irradiance zones, including irradiance zone of 1%. Each point represents an individual sample, and the circle size indicates the chlorophyll a concentration. (C) Relative importance of ecological processes driving the protistan assembly in SPG across the entire, euphotic, and aphotic zones.

Fig 4

Diel variability in relative sequence abundance of protistan trophic functional groups at order level based on 18S rRNA gene amplicon sequencing data in the central gyre region at station 8 in the vertical profile of 300 m over 24 hours at four time points: 2 a.m., 8 a.m., 2 p.m., and 9 p.m.

Fig 5

Partitioning of fungal major taxonomic groups and driving factors in South Pacific Gyre. (A) Relative sequence abundance of fungal classes per depth and sampling station. Classes with relative sequence abundance < 1% were aggregated into the group reported as “'Others.” (B) PCoA of fungal community diversity color coded by pelagic zones and number coded by the station. Pelagic zones: epipelagic (surface: 20–80 m, DCM: 100–250 m); mesopelagic: 300–500 m; and bathypelagic: 1,000–5,125 m. (C) Distance-decay relationship of Bray-Curtis and geographical distance (km) between sampling stations of fungal community at the ASV level (P < 0.001). The line represents a linear regression. (D) Mantel test correlation plot of fungi with environmental variables based on the Bray-Curtis distance.