The Role of Heterotrophic Bacteria and Archaea in the Transformation of Lignin in the Open Ocean

McDonald, Natasha; Achterberg, Eric P.; Carlson, Craig A.; Gledhill, Martha; Liu, Shuting; Matheson-Barker, Julia R; Nelson, N. B.; Parsons, Rachel

doi:10.3389/fmars.2019.00743

Cited by 15 publications

(8 citation statements)

References 62 publications

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“…However, their total abundance in the surface microcosms remained rather constant throughout the incubations, suggesting that they were not particularly active even when more labile substrates were available during the first 2 weeks of the incubation, which resembled bloom conditions at the study site ( 50 ). This apparent inactivity of Pelagibacter was also observed in other studies ( 44 , 50 ) and can also explain the slight difference in the relative abundance of the rare biosphere between the two deeper treatments (Fig. 4D) as Pelagibacter accounted for about 10% of the bathypelagic community near the end of the incubation.…”

Section: Discussionsupporting

confidence: 87%

“…We observed a slight decrease in CRAM abundance in all treatments, which was not anticipated in the “island of stability” ( 41 ). This consumption may be related to the composition of the prokaryotic communities, where several taxa (e.g., Euryarchaeota, Thaumarchaeota, and Rhodobacteraceae) observed in all treatments have been recently associated with the degradation of CRAM-like compounds ( 44 , 45 ). Nevertheless, CRAM relative abundance still represented about 65% of the ultrahigh mass spectrometry signal, and although not all CRAM-like compounds are refractory ( 45 ), this suggests that most of them have a refractory nature.…”

Section: Discussionmentioning

confidence: 99%

“…This production of new substrates by Thaumarcheota may help with the cometabolism of more recalcitrant DOM compounds by other microbial heterotrophs in the deeper treatments through priming ( 55 ). Some Thaumarcheota have also been shown to be mixotrophic ( 44 ), or even fully heterotrophic ( 56 ), and likely participate directly in DOM transformation as well. The other taxa, Colwelliaceae, is a family of Gammaproteobacteria known to grow in the deep ocean and is associated with the degradation of moderately complex DOM ( 57 ).…”

Section: Discussionmentioning

confidence: 99%

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Deep ocean microbial communities produce more stable dissolved organic matter through the succession of rare prokaryotes

et al. 2022

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The microbial carbon pump (MCP) hypothesis suggests that successive transformation of labile dissolved organic carbon (DOC) by prokaryotes produces refractory DOC (RDOC) and contributes to the long-term stability of the deep ocean DOC reservoir. We tested the MCP by exposing surface water from a deep convective region of the ocean to epipelagic, mesopelagic, and bathypelagic prokaryotic communities and tracked changes in dissolved organic matter concentration, composition, and prokaryotic taxa over time. Prokaryotic taxa from the deep ocean were more efficient at consuming DOC and producing RDOC as evidenced by greater abundance of highly oxygenated molecules and fluorescent components associated with recalcitrant molecules. This first empirical evidence of the MCP in natural waters shows that carbon sequestration is more efficient in deeper waters and suggests that the higher diversity of prokaryotes from the rare biosphere holds a greater metabolic potential in creating these stable dissolved organic compounds.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Deep ocean microbial communities produce more stable dissolved organic matter through the succession of rare prokaryotes

et al. 2022

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“…Our results show that microbial reworking of DOM, especially after exposure to light, can result in humification that is optically similar to fluorescent DOM (peaks A and C) traditionally viewed as terrestrial, in agreement with prior Arctic studies 7 . In this context, elevated concentrations of lignin phenols that still fall below a concentration threshold for microbial use could be observed alongside visible humic material derived from more accessible, potentially non-colored, terrestrial DOM, although the necessity of terrestrial source material is not clear from our dataset 25,49 . Our observations of an increasingly humic signal over time are consistent with observations of successive microbial processing to a diverse, "universal" aquatic DOM pool 50,51 as well as "universal" fluorescent signatures, consistent with similar functional processing of material by microbes to a convergent optical signature regardless of source 52 .…”

Section: Microbial Size Dependency Of Dom Diagenesis Microbial Transformations Of Dom Resulted In Threementioning

confidence: 86%

DOM degradation by light and microbes along the Yukon River-coastal ocean continuum

Grunert

Tzortziou

Neale

et al. 2021

Sci Rep

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The Arctic is experiencing rapid warming, resulting in fundamental shifts in hydrologic connectivity and carbon cycling. Dissolved organic matter (DOM) is a significant component of the Arctic and global carbon cycle, and significant perturbations to DOM cycling are expected with Arctic warming. The impact of photochemical and microbial degradation, and their interactive effects, on DOM composition and remineralization have been documented in Arctic soils and rivers. However, the role of microbes, sunlight and their interactions on Arctic DOM alteration and remineralization in the coastal ocean has not been considered, particularly during the spring freshet when DOM loads are high, photoexposure can be quite limited and residence time within river networks is low. Here, we collected DOM samples along a salinity gradient in the Yukon River delta, plume and coastal ocean during peak river discharge immediately after spring freshet and explored the role of UV exposure, microbial transformations and interactive effects on DOM quantity and composition. Our results show: (1) photochemical alteration of DOM significantly shifts processing pathways of terrestrial DOM, including increasing relative humification of DOM by microbes by > 10%; (2) microbes produce humic-like material that is not optically distinguishable from terrestrial humics; and (3) size-fractionation of the microbial community indicates a size-dependent role for DOM remineralization and humification of DOM observed through modeled PARAFAC components of fluorescent DOM, either through direct or community effects. Field observations indicate apparent conservative mixing along the salinity gradient; however, changing photochemical and microbial alteration of DOM with increasing salinity indicate changing DOM composition likely due to microbial activity. Finally, our findings show potential for rapid transformation of DOM in the coastal ocean from photochemical and microbial alteration, with microbes responsible for the majority of dissolved organic matter remineralization.

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“…It was surprising to find that some taxa that are typically considered to be chemoautotrophs, such as the SAR324 clade, Nitrospinaceae , and members of Thaumarchaeota i.e., archaea marine benthic group A, showed 13 C-DOM incorporation in this study. While we cannot rule out the possibility of “cross feeding,” several studies have reported flexible and opportunistic metabolic lifestyle of these chemoautotrophs: SAR324 contained genes for C1 metabolism ( Swan et al, 2011 ); a genomic study revealed genes for complete oxidation of sulfur-containing organic carbon substrates in Nitrospinaceae ( Friedrich, 2002 ); archaea have been shown to be capable of oxidizing urea, polyamine and lignin in microbial remineralization experiments, or taking up 13 C or 15 N labeled urea or 3 H leucine in SIP and FISH studies ( Baltar et al, 2010 ; Connelly et al, 2014 ; Orsi et al, 2016 ; Damashek et al, 2019 ; McDonald et al, 2019 ; Seyler et al, 2019 ), although other studies showed that Thaumarchaeota did not assimilate organic carbon ( Dekas et al, 2019 ). Urea concentrations in our Syn exudate PPL extract were indeed more than two-fold greater than concentrations measured in the Syn lysate and Syn lysate PPL extract and might explain the enriched 13 C signal resolved in the archaeal biomass only in Syn exudate PPL treatment.…”

Section: Discussionmentioning

confidence: 99%

Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability

et al. 2020

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Bacterioplankton consume about half of the dissolved organic matter (DOM) produced by phytoplankton. DOM released from phytoplankton consists of a myriad of compounds that span a range of biological reactivity from labile to recalcitrant. Linking specific bacterioplankton lineages to the incorporation of DOM compounds into biomass is important to understand microbial niche partitioning. We conducted a series of DNA-stable isotope probing (SIP) experiments using 13 C-labeled substrates of varying lability including amino acids, cyanobacteria lysate, and DOM from diatom and cyanobacteria isolates concentrated on solid phase extraction PPL columns (SPE-DOM). Amendments of substrates into Sargasso Sea bacterioplankton communities were conducted to explore microbial response and DNA-SIP was used to determine which lineages of Bacteria and Archaea were responsible for uptake and incorporation. Greater increases in bacterioplankton abundance and DOC removal were observed in incubations amended with cyanobacteria-derived lysate and amino acids compared to the SPE-DOM, suggesting that the latter retained proportionally more recalcitrant DOM compounds. DOM across a range of bioavailability was utilized by diverse prokaryotic taxa with copiotrophs becoming the most abundant 13 C-incorporating taxa in the amino acid treatment and oligotrophs becoming the most abundant 13 C-incorporating taxa in SPE-DOM treatments. The lineages that responded to SPE-DOM amendments were also prevalent in the mesopelagic of the Sargasso Sea, suggesting that PPL extraction of phytoplankton-derived DOM isolates compounds of ecological relevance to oligotrophic heterotrophic bacterioplankton. Our study indicates that DOM quality is an important factor controlling the diversity of the microbial community response, providing insights into the roles of different bacterioplankton in resource exploitation and efficiency of marine carbon cycling.

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The Role of Heterotrophic Bacteria and Archaea in the Transformation of Lignin in the Open Ocean

Abstract: Bacterioplankton and Terrigenous DOM lignin degradation. Our findings indicate that marine bacteria and archaea play a role in the transformation of the optical properties of lignin in the open ocean and that they may serve as a potential sink for a portion of the lignin macromolecule.

Cited by 15 publications

References 62 publications

Deep ocean microbial communities produce more stable dissolved organic matter through the succession of rare prokaryotes

Deep ocean microbial communities produce more stable dissolved organic matter through the succession of rare prokaryotes

DOM degradation by light and microbes along the Yukon River-coastal ocean continuum

Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability

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