Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions

Abstract

Biological interactions underpin the functioning of marine ecosystems, be it via competition, predation, mutualism, or symbiosis processes. Microbial phototroph-heterotroph interactions propel the engine that results in the biogeochemical cycling of individual elements and are critical for understanding and modelling global ocean processes. Unfortunately, studies thus far have focused on exponentially-growing cultures in nutrient-rich media, meaning knowledge of such interactions under in situ conditions is rudimentary at best. Here, we performed long-term phototroph-heterotroph co-culture experiments under nutrient-amended and natural seawater conditions which showed that it is not the concentration of nutrients but rather their circulation that maintains a stable interaction and a dynamic system. Using the Synechococcus-Roseobacter interaction as a model phototroph-heterotroph case study we show that whilst Synechococcus is highly specialised for carrying out photosynthesis and carbon-fixation it relies on the heterotroph to re-mineralise the inevitably leaked organic matter making nutrients circulate in a mutualistic system. In this sense we challenge the general belief that marine phototrophs and heterotrophs compete for the same scarce nutrients and niche space, but instead suggest these organisms more likely benefit from each other because of their different levels of specialization and complementarity within long-term stable-state systems.

Transcriptomic responses of the marine cyanobacterium Prochlorococcus to viral lysis products

“…In our experiments, Prochlorococcus MIT9313 was grown in nutrient‐replete conditions and this may explain why vDOM addition did not promote its growth. Our results were consistent with a recent study showing that the exponential growth of marine Synechococcus in nutrient‐replete conditions was not affected after DOM was added at an amount similar to what we used here (Christie‐Oleza et al ., ).…”

100 Days of marine Synechococcus–Ruegeria pomeroyi interaction: A detailed analysis of the exoproteome

“…WH7803 and R. pomeroyi DSS‐3 during the 100 days co‐culture in both natural oligotrophic seawater (SW) and enriched artificial seawater (ASW) (Fig. ) showed the expected trends as previously reported (Christie‐Oleza et al ., ). While Synechococcus sp.…”

“…Synechococcus sp. release considerable amounts of organic matter not only in the form of carbohydrates (Biersmith and Benner, ; Bertlisson et al ., ) but also in the form of protein (Christie‐Oleza et al ., ; ). Here, proteins involved in photosynthesis are among the most abundant categories found in the exoproteome of Synechococcus sp.…”

“…Despite being outnumbered by the heterotrophic community, these cyanobacteria are responsible for half of the marine primary production and play a key role in sustaining marine food webs (Falkowski, ). Hence, phytoplankton are at the base of the marine food chain feeding the ecosystem with DOM and POM that is released via cell lysis (e.g., cell death, inefficient grazing and viral lysis) or other cellular processes (e.g., outer membrane vesicles, active efflux processes or permeable membrane leakage) (Biller et al ., ; Christie‐Oleza et al ., ; Grossowicz et al ., ). Most of this organic matter will be used by the heterotrophic bacterioplankton as their main source of carbon and energy, returning inorganic nutrients to the phototrophic community (Christie‐Oleza et al ., ).…”

The interactions of an algae–fungi symbiotic system influence nutrient removal from synthetic wastewater

“…In addition, the interaction between fungi and algae during wastewater treatment remains unclear. The general belief that microbes compete for the same scare resources, while nutrients recycling among microbes may facilitate stability of microbial stable‐state system . Performance and stability of symbiotic system had not been studied when encountering nutrients variation in wastewater.…”