Hidden in plain sight: The importance of cryptic interactions in marine plankton

Millette, Nicole C.; Große, Julia; Johnson, Winifred M.; Jungbluth, Michelle J.; Suter, Elizabeth A.

doi:10.1002/lol2.10084

Cited by 11 publications

(9 citation statements)

References 90 publications

(256 reference statements)

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“…The inability of an organism to synthesize a particular compound required for its growth (auxotrophy) appears to be more widespread than previously assumed (Millette et al ., ). Exploiting a resource produced by another organism rather than de novo synthesizing a specific compound has been suggested to provide a selective advantage leading to reductive genome evolution (‘Black Queen Hypothesis’) (Morris et al ., ).…”

Section: Resultsmentioning

confidence: 97%

Ammonia‐oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Bayer

Hansman

Bittner

et al. 2019

Environmental Microbiology

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Summary Ammonia‐oxidizing archaea (AOA) constitute a considerable fraction of microbial biomass in the global ocean, comprising 20%–40% of the ocean's prokaryotic plankton. However, it remains enigmatic to what extent these chemolithoautotrophic archaea release dissolved organic carbon (DOC). A combination of targeted and untargeted metabolomics was used to characterize the exometabolomes of three model AOA strains of the Nitrosopumilus genus. Our results indicate that marine AOA exude a suite of organic compounds with potentially varying reactivities, dominated by nitrogen‐containing compounds. A significant fraction of the released dissolved organic matter (DOM) consists of labile compounds, which typically limit prokaryotic heterotrophic activity in open ocean waters, including amino acids, thymidine and B vitamins. Amino acid release rates corresponded with ammonia oxidation activity and the three Nitrosopumilus strains predominantly released hydrophobic amino acids, potentially as a result of passive diffusion. Despite the low contribution of DOC released by AOA (~0.08%–1.05%) to the heterotrophic prokaryotic carbon demand, the release of physiologically relevant metabolites could be crucial for microbes that are auxotrophic for some of these compounds, including members of the globally abundant and ubiquitous SAR11 clade.

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Section: Resultsmentioning

confidence: 97%

Ammonia‐oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Bayer

Hansman

Bittner

et al. 2019

Environmental Microbiology

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“…However, no global agreement has been reached on to what extent the different mixotypes should be modeled. This is mainly due to a lack of quantitative and comparative data on the global impact of grazing and carbon fixation by the different mixotypes [75]. With our study, we show how meta-omics data can be used to identify groups of organisms distributed differently in response to the environment.…”

Section: Towards An Integration Of Mixotrophic Diversity Into Marine mentioning

confidence: 86%

Mixotrophic protists display contrasted biogeographies in the global ocean

et al. 2019

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Mixotrophy, or the ability to acquire carbon from both auto-and heterotrophy, is a widespread ecological trait in marine protists. Using a metabarcoding dataset of marine plankton from the global ocean, 318,054 mixotrophic metabarcodes represented by 89,951,866 sequences and belonging to 133 taxonomic lineages were identified and classified into four mixotrophic functional types: constitutive mixotrophs (CM), generalist non-constitutive mixotrophs (GNCM), endo-symbiotic specialist non-constitutive mixotrophs (eSNCM), and plastidic specialist non-constitutive mixotrophs (pSNCM). Mixotrophy appeared ubiquitous, and the distributions of the four mixotypes were analyzed to identify the abiotic factors shaping their biogeographies. Kleptoplastidic mixotrophs (GNCM and pSNCM) were detected in new zones compared to previous morphological studies. Constitutive and non-constitutive mixotrophs had similar ranges of distributions. Most lineages were evenly found in the samples, yet some of them displayed strongly contrasted distributions, both across and within mixotypes. Particularly divergent biogeographies were found within endo-symbiotic mixotrophs, depending on the ability to form colonies or the mode of symbiosis. We showed how metabarcoding can be used in a complementary way with previous morphological observations to study the biogeography of mixotrophic protists and to identify key drivers of their biogeography.

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“…Furthermore, the inability of an organism to synthesize a particular compound required for its growth (auxotrophy) appears to be more widespread than previously assumed 68 . Exploiting a resource produced by another organism rather than de novo synthesizing a specific compound has been suggested to provide a selective advantage leading to reductive genome evolution (“Black Queen Hypothesis”) 69 .…”

Section: Resultsmentioning

confidence: 99%

Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Bayer

Hansman

Bittner

et al. 2019

Preprint

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24 Ammonia-oxidizing archaea (AOA) constitute a considerable fraction of microbial biomass in 25 the global ocean, comprising 20-40% of the ocean's prokaryotic plankton and thus play an 26 important role in global nitrogen cycle. However, it remains enigmatic to what extent these 27 chemolithoautotrophic archaea are releasing dissolved organic matter (DOM). A combination 28 of targeted and untargeted metabolomics was used to characterise the exometabolomes of 29 three model AOA strains of the Nitrosopumilus genus. Furthermore, we compared the 30 composition of intra-and extracellular dissolved free amino acids (DFAA). Our results indicate 31 that marine AOA exude a suite of organic compounds with potentially varying reactivity, 32 dominated by nitrogen-containing compounds. A significant fraction of the released DOM 33 consisted of labile compounds, which typically limit prokaryotic heterotrophic activity in open 34 ocean waters, including amino acids, thymidine and B vitamins. In growing Nitrosopumilus 35 cultures, hydrophobic amino acids were likely released as a result of passive diffusion 36 corresponding to ammonia oxidation activity, while glycine was continuously released at high 37 rates. Our results suggest that AOA release several ecologically and biochemically relevant 38 metabolites, potentially fueling heterotrophic prokaryotes in the ocean.39 40 42 magnitude to atmospheric CO2 and of major significance for the global carbon cycle and 43 climate 1,2 . DOM is highly complex, consisting of thousands of different organic molecules 3,4 44 and comprising the most heterogeneous and dynamic pool of carbon in the oceans 5 . Its 45 concentration and composition are affected by biotic processes such as photosynthesis and 46 heterotrophic metabolism 6,7 , as well as by photochemical processes 8 . However, while the flux 47 of carbon through this pool of molecules is mediated largely by microbial activity, the 48 relationships between marine microbes and the molecules making up the DOM pool remain 49 poorly characterized 9 .50 3 DOM is released as a by-product of metabolically active microbes, but may also be 51 released for nutrient acquisition and communication (in the forms of metal-binding ligands and 52 quorum sensing chemicals, respectively) 6,10,11 , as well as upon predation or viral lysis 12 . The 53 fraction of DOM exuded by phytoplankton is highly variable accounting for 5 -70% of 54 photosynthetically fixed carbon 6 . There are major gaps, however, in our understanding of the 55 biogeochemical significance of the released compounds 13 . The composition of DOM released 56 by heterotrophic bacteria is even less known than for phytoplankton, however, they do 57 produce and release organic compounds for similar purposes as phytoplankton 5,6,14,15 . 58 Although the largest fraction of DOM remains uncharacterized with respect to 59 molecular identity, phytoplankton exudates consist to a considerable extent of labile 60 compounds such as carbohydrates (mono-, and polysaccharides), proteins and amino acids ...

show abstract

Hidden in plain sight: The importance of cryptic interactions in marine plankton

Cited by 11 publications

References 90 publications

Ammonia‐oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Ammonia‐oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Mixotrophic protists display contrasted biogeographies in the global ocean

Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

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