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Trophic complexity in aqueous systems: bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen removal.

ABSTRACT: Loading of water bodies with dissolved organic carbon (DOC) and dissolved total nitrogen (DTN) affects their integrity and functioning. Microbial interactions mitigate the negative effects of high nutrient loads in these ecosystems. Despite numerous studies on how biodiversity mediates ecosystem functions, whether and how diversity and complexity of microbial food webs (horizontal, vertical) and the underlying ecological mechanisms influence nutrient removal has barely been investigated. Using microbial microcosms accommodating systematic combinations of prey (bacteria) and predator (protists) species, we showed that increasing bacterial richness improved the extent and reliability of DOC and DTN removal. Bacterial diversity drove nutrient removal either due to species foraging physiology or functional redundancy, whereas protistan diversity affected nutrient removal through bacterial prey resource partitioning and changing nutrient balance in the system. Our results demonstrate that prey-predator diversity and trophic interactions interactively determine nutrient contents, thus implying the vital role of microbial trophic complexity as a biological buffer against DOC and DTN.

SUBMITTER: Saleem M

PROVIDER: S-EPMC4810830 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Trophic complexity in aqueous systems: bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen removal.

Saleem Muhammad M Fetzer Ingo I Harms Hauke H Chatzinotas Antonis A

Proceedings. Biological sciences 20160201 1825

Loading of water bodies with dissolved organic carbon (DOC) and dissolved total nitrogen (DTN) affects their integrity and functioning. Microbial interactions mitigate the negative effects of high nutrient loads in these ecosystems. Despite numerous studies on how biodiversity mediates ecosystem functions, whether and how diversity and complexity of microbial food webs (horizontal, vertical) and the underlying ecological mechanisms influence nutrient removal has barely been investigated. Using m ...[more]

PMID: 26888033

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Project description:BackgroundRecent advances in sequencing strategies make possible unprecedented depth and scale of sampling for molecular detection of microbial diversity. Two major paradigm-shifting discoveries include the detection of bacterial diversity that is one to two orders of magnitude greater than previous estimates, and the discovery of an exciting 'rare biosphere' of molecular signatures ('species') of poorly understood ecological significance. We applied a high-throughput parallel tag sequencing (454 sequencing) protocol adopted for eukaryotes to investigate protistan community complexity in two contrasting anoxic marine ecosystems (Framvaren Fjord, Norway; Cariaco deep-sea basin, Venezuela). Both sampling sites have previously been scrutinized for protistan diversity by traditional clone library construction and Sanger sequencing. By comparing these clone library data with 454 amplicon library data, we assess the efficiency of high-throughput tag sequencing strategies. We here present a novel, highly conservative bioinformatic analysis pipeline for the processing of large tag sequence data sets.ResultsThe analyses of ca. 250,000 sequence reads revealed that the number of detected Operational Taxonomic Units (OTUs) far exceeded previous richness estimates from the same sites based on clone libraries and Sanger sequencing. More than 90% of this diversity was represented by OTUs with less than 10 sequence tags. We detected a substantial number of taxonomic groups like Apusozoa, Chrysomerophytes, Centroheliozoa, Eustigmatophytes, hyphochytriomycetes, Ichthyosporea, Oikomonads, Phaeothamniophytes, and rhodophytes which remained undetected by previous clone library-based diversity surveys of the sampling sites. The most important innovations in our newly developed bioinformatics pipeline employ (i) BLASTN with query parameters adjusted for highly variable domains and a complete database of public ribosomal RNA (rRNA) gene sequences for taxonomic assignments of tags; (ii) a clustering of tags at k differences (Levenshtein distance) with a newly developed algorithm enabling very fast OTU clustering for large tag sequence data sets; and (iii) a novel parsing procedure to combine the data from individual analyses.ConclusionOur data highlight the magnitude of the under-sampled 'protistan gap' in the eukaryotic tree of life. This study illustrates that our current understanding of the ecological complexity of protist communities, and of the global species richness and genome diversity of protists, is severely limited. Even though 454 pyrosequencing is not a panacea, it allows for more comprehensive insights into the diversity of protistan communities, and combined with appropriate statistical tools, enables improved ecological interpretations of the data and projections of global diversity.

Project description:Knowledge about the primary factor controlling stable isotope ratios of particulate nitrogen (?15NPN) and total dissolved nitrogen (?15NTDN) in a subtropical reservoir can improve the understanding of regional and global nitrogen cycles. Taking Lianhe Reservoir as a representative subtropical reservoir, we studied the spatial and temporal distributions of ?15NPN and?15NTDN and their relationships with the surrounding physicochemical factors and phytoplankton. The results showed that variations in ?15NPN and ?15NTDN followed seasonal thermal cycles. The values of ?15NTDN were inversely proportional to those of ?15NPN. PCA showed that phytoplankton cell density and pH were the primary drivers of the variation of ?15NPN (45.2%). The primary factors influencing ?15NTDN were Chl a and phytoplankton cell density, which both indicated phytoplankton biomass. We also determined that the dominant species was Microcystis densa during the thermal stratification period and Staurodesmus aristiferus during the mixing period. Laboratory experiments showed that ?15NPN values in both M. densa (from 19.5 to 14.6‰) and S. aristiferus (from 19.4 to 16.0 ‰) media decreased significantly as the algal cells grew. Furthermore, the ?15NTDN values increased from 4.9 to 7.9‰ and from 4.7 to 6.9‰ in M. densa and S. aristiferus media, respectively, when the ?15NPN values decreased. These experimental results were consistent with field investigation results and indicated that variations in ?15NPN and ?15NTDN were mainly controlled by phytoplankton cell density, especially the cell density of the dominant species, in both the thermal stratification and mixing periods. The results also suggested that cell density, not phytoplankton species, was the key factor regulating the distribution of nitrogen stable isotopes. These results together indicated that phytoplankton cell density is the primary factor in the regulation of nitrogen stable isotope composition and that its influence is greater than that of other physical and chemical factors. This study provided detailed information supporting the primary role of phytoplankton in the nitrogen geochemical cycle and improved the understanding of biochemical processes in natural subtropical reservoirs.

Dataset Information

Trophic complexity in aqueous systems: bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen removal.

Publications

Trophic complexity in aqueous systems: bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen removal.

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