bioRxiv Science⌕ Search

Biology subjects

Eigemann, F.

Publications and source records attributed to Eigemann, F..

6 recordsLinked to original sources

Heterotrophic prokaryotes internal carbon recycling compensates mismatches between phytoplankton production and heterotrophic prokaryotic consumption

Molecular observational tools are great for characterizing the composition and genetic endowment of microbial communities, but cannot measure fluxes, which are critical for the understanding of ecosystems. To overcome these limitations, we use a mechanistic inference approach to estimate dissolved organic carbon (DOC) production and consumption by phytoplankton operational taxonomic units (OTUs) and heterotrophic prokaryotic amplicon sequences variants (ASVs), and infer carbon fluxes between members of this microbial community from Western English Channel (WEC) time-series data. Our analyses focus on phytoplankton spring and summer blooms, as well as bacteria summer blooms. In spring blooms, phytoplankton DOC production exceeds heterotrophic prokaryotic consumption, but in bacterial summer blooms heterotrophic prokaryotes consume almost 3 times more DOC than produced by the phytoplankton. This mismatch is compensated by heterotrophic prokaryotic DOC release by death, presumably viral lysis. In both types of summer blooms, large amounts of the DOC liberated by heterotrophic prokaryotes are reused, i.e. internally recycled, and fluxes between different heterotrophic prokaryotes are at the same level as fluxes between phytoplankton and heterotrophic prokaryotes. Contextualized, internal recycling accounts for approximately 75% and 30% of the estimated net primary production (0.16 vs 0.22 and 0.08 vs 0.29 {micro}mol l-1 d-1) in bacteria and phytoplankton summer blooms, respectively, and thus represents a major component of the WEC carbon cycle. We conclude that internal recycling compensates mismatches between phytoplankton DOC production and heterotrophic prokaryotic consumption, and encourage future analyses on aquatic carbon cycles to consider fluxes between heterotrophic prokaryotes, i.e. internal recycling.

microbiology↗

An Interplay of Phytoplankton Donor Species and Transformation of Released Compounds over Time Defines Bacterial Communities Following Phytoplankton DOMp Pulses

Phytoplankton-bacteria interactions are stimulated by phytoplankton-released dissolved organic matter (DOMp). Two factors that shape the accompanying bacterial community are i) the "donor" phytoplankton species, defining the initial composition of released DOMp, and ii) the DOMp transformation over time. We added phytoplankton DOM from two globally abundant species - the diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus MIT9312 - to natural bacterial communities in the Eastern Mediterranean and determined the bacterial responses over a time-course of 72 h in terms of cell numbers, bacterial production (BP), alkaline phosphatase activity (APA), and changes in active bacterial community compositions based on rRNA amplicon sequencing. Both DOMp types were demonstrated to serve the bacterial community as carbon and potentially phosphorus source. Diatom-derived DOM induced higher BP and lower APA compared to cyanobacterium DOM after 24 h, but not after 48 and 72 h of incubation, and also maintained higher Shannon diversities over the course of the experiment, indicating a better bacterial accessibility and broader disposability of diatom derived DOM. Bacterial communities significantly differed between DOMp types as well as different incubation times, pointing to a certain bacterial specificity for the DOMp donor as well as a successive utilization of phytoplankton DOM by different bacterial taxa. The highest differences in bacterial community composition with DOMp types occurred shortly after additions, suggesting a high specificity towards highly bioavailable DOMp compounds. We conclude that phytoplankton associated bacterial communities are strongly shaped by an interplay between phytoplankton donor and the transformation of its released DOMp over time. IMPORTANCEPhytoplankton-bacteria interactions maintain biogeochemical cycles of global importance. Phytoplankton photosynthetically fix carbon dioxide and subsequently release the synthesized compounds as dissolved organic matter (DOMp), which becomes processed and recycled by heterotrophic bacteria. Yet, the combined effect of the phytoplankton donor species and time-dependent transformation of DOMp compounds on the accessibility to the bacterial community has not been explored until now. The diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus MIT9312 are globally important phytoplankton species, and our study revealed that DOMp of both species was selectively incorporated by the bacterial community. The donor species had the highest impact shortly after DOMp appropriation, and its effect diminished over time. Our results improve the understanding of biogeochemical cycles between phytoplankton and bacteria, and solve yet unresolved questions of phytoplankton-bacteria interactions.

microbiology↗

Significant organic carbon acquisition by Prochlorococcus in the oceans

Marine phytoplankton are responsible for about half of the photosynthesis on Earth. Many are mixotrophs, combining photosynthesis with heterotrophic assimilation of organic carbon but the relative contribution of these two carbon sources is not well quantified. Here, single-cell measurements reveal that Prochlorococcus at the base of the photic zone in the Eastern Mediterranean Sea are obtaining only ~20% of carbon required for growth by photosynthesis. Consistently, laboratory-calibrated evaluations of Prochlorococcus photosynthesis indicate that carbon fixation is systematically too low to support published in situ growth rates in the deep photic layer of the Pacific Ocean. Furthermore, agent-based model simulations show that mixotrophic cells maintain realistic growth rates and populations 10s of meters deeper than obligate photo-autotrophs, deepening the nutricline and Deep Chlorophyll Maximum by ~20 m. Time-series of Prochlorococcus ecotype-abundance from the subtropical North Atlantic and North Pacific suggest that up to 30% of the Prochlorococcus cells live where light intensity is not enough to sustain obligate photo-autotrophic populations during warm, stratified periods. Together, these data and models suggest that mixotrophy underpins the ecological success of a large fraction of the global Prochlorococcus population and its collective genetic diversity.

microbiology↗

Phytoplankton exudates provide full nutrition to a subset of accompanying heterotrophic bacteria via carbon, nitrogen and phosphorus allocation

Marine bacteria rely on phytoplankton exudates as carbon sources (DOCp). Yet, it is unclear to what extent phytoplankton exudates also provide nutrients such as phytoplankton-derived N and P (DONp, DOPp). We address these questions by exudate addition experiments from the ubiquitous pico-cyanobacterium Prochlorococcus to contrasting ecosystems in the Eastern Mediterranean - a coastal and an open-ocean, oligotrophic station. Nutrient addition did not lower the incorporation of exudate DONp, nor did it reduce alkaline phosphatase activity, suggesting that bacterial communities are able to exclusively cover their nitrogen and phosphorus demands with organic forms provided by phytoplankton exudates. Approximately half of the cells in each ecosystem took up detectable amounts of Prochlorococcus-derived C and N, yet based on 16S rRNA sequencing different bacterial genera were responsible for the observed exudate utilization patterns. In the coastal community, several phylotypes of Aureimarina, Psychrosphaera and Glaciecola responded positively to the addition of phytoplankton exudates, whereas phylotypes of Pseudoalteromonas increased and dominated the open ocean communities. Together, our results strongly indicate that phytoplankton exudates provide coastal and open-ocean bacterial communities with organic carbon, nitrogen and phosphorus, and that phytoplankton exudate serve a full-fledged meal for specific members of the accompanying bacterial community in the nutrient-poor eastern Mediterranean.

ecology↗

Distinctive tasks of different cyanobacteria and associated bacteria in carbon as well as nitrogen fixation and cycling in a late stage Baltic Sea bloom

Cyanobacteria and associated heterotrophic bacteria hold key roles in carbon as well as nitrogen fixation and cycling in the Baltic Sea due to massive cyanobacterial blooms each summer. The species specific activities of different cyanobacterial species as well as the N- and C-exchange of associated heterotrophic bacteria in these processes, however, are widely unknown. Within one time series experiment we tested the cycling in a natural, late stage cyanobacterial bloom by adding 13C bi-carbonate and 15N2, and performed sampling after 10 min, 30 min, 1 h, 6 h and 24 h in order to determine the fixing species as well as the fate of the fixed carbon and nitrogen in the associations. Uptake of 15N and 13C isotopes by the most abundant cyanobacterial species as well as the most abundant associated heterotrophic bacterial groups was then analysed with a NanoSIMS. Overall, the filamentous, heterocystous species Dolichospermum sp., Nodularia sp., and Aphanizomenon sp. revealed no or erratic uptake of carbon and nitrogen, indicating mostly inactive cells. In contrary, non-heterocystous Pseudanabaena sp. dominated the nitrogen and carbon fixation, with uptake rates up to 1.49 {+/-} 0.47 nmol N h-1 l-1 and 2.55 {+/-} 0.91 nmol C h-1 l-1. Associated heterotrophic bacteria dominated the subsequent nitrogen cycling with uptake rates up to 1.2 {+/-} 1.93 fmol N h-1 cell -1, but were also indicative for fixation of di-nitrogen.

ecology↗

Prochlorococcus rely on microbial interactions rather than on chlorotic resting stages to survive long-term stress

Many microorganisms produce resting cells with very low metabolic activity that allow them to survive phases of prolonged nutrient or energy stress. In cyanobacteria and some eukaryotic phytoplankton, the production of resting stages is accompanied by a loss of photosynthetic pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. In Prochlorococcus strain MIT9313, chlorotic cells show reduced metabolic activity, measured as C and N uptake by NanoSIMS. However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not re-grow under axenic conditions when transferred to new media. Nevertheless, co-cultures with a heterotrophic bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of Prochlorococcus. ImportanceThe ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions as is common in nature. Therefore, one would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. Here, we show that this is not the case for Prochlorococcus, a globally abundant and ecologically impactful marine cyanobacterium. Instead, Prochlorococcus rely on co-occurring heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean and elsewhere with consequences at the global scale.

microbiology↗