Novel Interactions Between Phytoplankton and Bacteria Shape Microbial Seasonal Dynamics in Coastal Ocean Waters

Abstract

Trophic interactions between marine phytoplankton and heterotrophic bacteria are at the base of the biogeochemical carbon cycling in the ocean. However, the specific interactions taking place between phytoplankton and bacterial taxa remain largely unexplored, particularly out of phytoplankton blooming events. Here, we applied network analysis to a 3.5-year time-series dataset to assess the specific associations between different phytoplankton and bacterial taxa along the seasonal scale, distinguishing between free-living and particle-attached bacteria. Using a newly developed network post-analysis technique we removed bacteria-phytoplankton correlations that were primarily driven by environmental parameters, to detect potential biotic interactions. Our results indicate that phytoplankton dynamics may be a strong driver of the inter-annual variability in bacterial community composition. We found the highest abundance of specific bacteria-phytoplankton associations in the particle-attached fraction, indicating a tighter bacteria-phytoplankton association than in the free-living fraction. In the particle-associated fraction we unveiled novel potential associations such as the one between Planctomycetes taxa and the diatom Leptocylindrus spp. Consistent correlations were also found between free-living bacterial taxa and different diatoms, including novel associations such as those between SAR11 with Naviculales diatom order, and between Actinobacteria and Cylindrotheca spp. We also confirmed previously known associations between Rhodobacteraceae and Thalassiosira spp. Our results expand our view on bacteria-phytoplankton associations, suggesting that taxa-specific interactions may largely impact the seasonal dynamics of heterotrophic bacterial communities.

Temporal variability in the growth-enhancing effects of different bacteria within the microbiome of the diatom Actinocyclus sp.

“…A wide diversity of bacterial taxa are commonly associated with diatoms both in culture conditions ( Amin et al, 2012 ; Ajani et al, 2018 ; Crenn et al, 2018 ; Mönnich et al, 2020 ) and in natural aquatic environments ( Teeling et al, 2012 ; Arandia-Gorostidi et al, 2022 ). However, whilst the ecological and metabolic interactions involved in a handful of diatom-bacteria model systems have been characterised ( Amin et al, 2015 ; Durham et al, 2015 , 2017 ; Ferrer-González et al, 2021 ; Olofsson et al, 2022 ), the impacts of diatom-associated bacteria on host growth are still largely unknown.…”

Dissecting host‐microbiome interaction effects on phytoplankton microbiome composition and diversity

“…A focus on particle‐associated bacteria may be warranted as they play an important role in the remineralisation of organic matter, which is one of the potential forces to drive the bacteria‐phytoplankton mutualistic interaction (Parveen et al, 2013). Particle‐associated bacteria also exert a more direct interaction with their host due to their physical attachment to the phytoplankton surface, as has been suggested before (Ahern et al, 2021; Arandia‐Gorostidi et al, 2022; Schweitzer‐Natan et al, 2019). Consequently, particle‐associated bacteria may have a stronger association with host‐microbiome feedback effects compared to free‐living bacterial communities.…”

Dynamics of Prokaryotes in the Arabian Sea: Insights into the Interplay of Physicochemical and Biological Variables from Epi to Bathypelagic zone

“…The primary source of dissolved organic matter for bacterial metabolism is phytoplankton, obtained through the release from healthy cells, breakdown of senescent or dead cells and zooplankton feeding (Irwin et al, 2006;Landry et al, 2002). This establishes a dependable correlation between the abundance of bacteria and phytoplankton and their production (Liu et al, 2014;Rooney-Varga et al, 2005;Arandia-Gorostidi et al, 2022).…”

“…Seasonal monsoonal wind reversals, and upwelling produce exceptionally high amounts of primary productivity in the Arabian Sea (Wiggert et al, 2005;Parab et al, 2006;(Gerson et al, 2014); Jyothibabu et al, 2021;Chowdhury et al, 2021). The phytoplankton-released compounds, as well as other environmental variables, affect the number and composition of microbial communities over time and space (Arandia-Gorostidi et al, 2022;(Caroppo et al, 2022;Fernandes & Bogati, 2022;Sison-Mangus et al, 2016).…”