Evidence of the Significant Contribution of Heterotrophic Diazotrophs to Nitrogen Fixation in the Eastern Indian Ocean During Pre-Southwest Monsoon Period

Wu, Chao; Sun, Jun; Liu, Haijiao; Xu, Wenzhe; Zhang, Guicheng; Lu, Hanfang; Guo, Yiyan

doi:10.1007/s10021-021-00702-z

Cited by 12 publications

(21 citation statements)

References 80 publications

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“…These predictions were partially supported by several field measurements showing that high nitrogen fixation rates occur off the Australian continent (Messer et al., 2016; Raes et al., 2014, 2015). However, most field measurements in the EIO commonly show low nitrogen fixation with a dominance of heterotrophic bacterial diazotrophs (Löscher et al., 2020; Sarma et al., 2020; Saxena et al., 2020; Wu et al., 2019, 2021), indicating that simple extrapolation of the knowledge in the Pacific and Atlantic is not applicable to the EIO to simulate the biological nitrogen fixation activity pattern.…”

Section: Introductionmentioning

confidence: 99%

Low Nitrogen Fixation Related to Shallow Nitracline Across the Eastern Indian Ocean

et al. 2022

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Nitrogen fixation by diazotrophs provides a substantial source of bioavailable nitrogen in the ocean, supporting new production and net carbon uptake in the ocean (Gruber & Galloway, 2008;Karl et al., 1997). In the past two decades, sequencing of the nifH gene (which encodes the iron unit of nitrogenase) has revealed diverse diazotrophs, including cyanobacteria such as Trichodesmium and UCYN-A1, and non-cyanobacteria with broad geographic ranges from tropical and subtropical to polar regions (Zehr & Capone, 2020).The elucidation of the diversity of diazotrophs has shown that various factors control the activity and community structure of diazotrophs, including temperature, phosphorus, iron, nutrient supply ratios, and zooplankton grazing (

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Section: Introductionmentioning

confidence: 99%

Low Nitrogen Fixation Related to Shallow Nitracline Across the Eastern Indian Ocean

et al. 2022

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“…However, denitrification and anammox were all suppressed in the surface waters, and the net results were that nitrogen fixation supplied fixed nitrogen in the upper layers. Our previous study using an isotope 15 N tracer technique also showed that nitrogen fixation rates were high in surface waters in the BoB and the southeastern Indian Ocean ( Wu et al, 2022b ). Overall, our study demonstrated that nitrogen fixation is significantly important in adding new nitrogen to the upper layers of this oligotrophic marine ecosystem.…”

Section: Discussionmentioning

confidence: 87%

“…This was quite different from our earlier study conducted during the spring inter-monsoon, where Trichodesmium spp. were dominant in the surface waters of the BoB ( Wu et al, 2019 , 2022b ). Wind-drift current was thought to be the main factor that influences the seasonal rhythm of Trichodesmium spp.…”

Section: Discussionmentioning

confidence: 99%

Diversity, structure, and distribution of bacterioplankton and diazotroph communities in the Bay of Bengal during the winter monsoon

Narale

Cui

et al. 2022

Front. Microbiol.

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The Bay of Bengal (BoB) is conventionally believed to be a low productive, oligotrophic marine ecosystem, where the diazotroph communities presumed to play a vital role in adding “new” nitrogen through the nitrogen fixation process. However, the diazotroph communities in the oceanic region of the BoB are still poorly understood though it represents most of the seawater volume. The present study investigated a detailed account of the bacterioplankton community structure and distribution in the oceanic BoB during the winter monsoon using high throughput sequencing targeting the 16S rRNA and nifH genes. Our study observed diverse groups of bacterioplankton communities in the BoB including both cyanobacterial and non-cyanobacterial phylotypes. Cyanobacteria (Prochlorococcus spp. and Synechococcus spp.) and Proteobacteria (mainly α-, γ-, and δ-Proteobacteria) were the most abundant groups within the bacterial communities, possessing differential vertical distribution patterns. Cyanobacteria were more abundant in the surface waters, whereas Proteobacteria dominated the deeper layers (75 m). However, within the diazotroph communities, Proteobacteria (mainly γ-Proteobacteria) were the most dominant groups than Cyanobacteria. Function prediction based on PICRUSt revealed that nitrogen fixation might more active to add fixed nitrogen in the surface waters, while nitrogen removal pathways (denitrification and anammox) might stronger in deeper layers. Canonical correspondence analysis (CCA) indicated that temperature, salinity, and silicate were major environmental factors driving the distribution of bacterial communities. Additionally, phosphate was also an important factor in regulating the diazotroph communities in the surface water. Overall, this study provided detailed information on bacterial communities and their vital role in the nitrogen cycles in oligotrophic ecosystems.

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“…In the warm, oligotrophic open ocean, these low nitrogen concentrations select for nitrogen-fixing organisms that can efficiently convert atmospheric N 2 to bioavailable NH 4 or amino acids (2). While our understanding of nitrogen-fixing organisms in the oceans is evolving to include nonautotrophic diazotrophs and other unexpected physiologies (e.g., (3)(4)(5)), the filamentous, colony-forming cyanobacterium Trichodesmium is still considered a critical oceanic nitrogen fixer (3,6).…”

Section: Significance Statementmentioning

confidence: 99%

“…4.1(101), matching Sequence Alignment/Map (SAMs) were converted to binary alignment maps (BAMs) with SAMtools v1.11(102), and BAMs were profiled across the TriCoLim read sets using Anvi'o to determine environmental auxiliary and environmental core genes (EAG and ECG, respectively). COG categories per 100kb was determined by exporting the annotation from Anvi'o, determining the COG categories per MAG, summing those results per clade, and then analyzing and graphing in R v 4.0.3 (2020-10-10) with R Studio v1.4.1103 (103).Differences between COG category counts per clades were tested for statistical significance using ANOVA in the R package rstatix(104).…”

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confidence: 99%

Importance of Mobile Genetic Element Immunity in Numerically AbundantTrichodesmiumClades

Webb

Held

Zhao

et al. 2022

Preprint

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The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient, open ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe the genetic potential of the genus via significantly improved genomic assemblies of strains Trichodesmium thiebautii H94, Trichodesmium erythraeum 2175, and 17 new Trichodesmium metagenome-assembled genomes (MAGs, >50% complete) from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ∼four N2 fixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas hereafter). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes and MAGs, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Multiple lines of evidence indicate that the CRISPR-Cas system is functional in situ: 1. Trichodesmium CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified, 2. High Trichodesmium spacer sequence variability indicating rapid adaptation, and 3. metaproteomic and transcriptomic expression analyses detecting the CRISPR-Cas system components in Trichodesmium colonies from the Atlantic and Pacific Oceans. These data suggest that phage or mobile genetic element immunity in T. thiebautii could contribute to their success, gene diversity, and numerical dominance over T. erythraeum in the oceans, thus warranting further Trichodesmium virome investigations.Significance statementOur work identifies CRISPR-Cas immunity as a phylogenetically distinct, environmentally expressed factor in the speciation of closely related N2-fixing Trichodesmium clades. These findings suggest that differential phage predation and resistance could be a previously overlooked selective pressure in the genus, potentially leading to the current numerical dominance of T. thiebautii over T. erythraeum in the oceans. Furthermore, while the currently CO2-limited T. erythraeum is expected to be a ‘winner’ of anthropogenic climate change, their predicted higher phage sensitivity than T. thiebautii could challenge this outcome.

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Evidence of the Significant Contribution of Heterotrophic Diazotrophs to Nitrogen Fixation in the Eastern Indian Ocean During Pre-Southwest Monsoon Period

Cited by 12 publications

References 80 publications

Low Nitrogen Fixation Related to Shallow Nitracline Across the Eastern Indian Ocean

Low Nitrogen Fixation Related to Shallow Nitracline Across the Eastern Indian Ocean

Diversity, structure, and distribution of bacterioplankton and diazotroph communities in the Bay of Bengal during the winter monsoon

Importance of Mobile Genetic Element Immunity in Numerically AbundantTrichodesmiumClades

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