The Microbial Carbon Pump: from Genes to Ecosystems

Abstract

The majority of marine dissolved organic carbon (DOC) is resistant to biological degradation and thus can remain in the water column for thousands of years, constituting carbon sequestration in the ocean. To date the origin of such recalcitrant DOC (RDOC) is unclear. A recently proposed conceptual framework, the microbial carbon pump (MCP), emphasizes the microbial transformation of organic carbon from labile to recalcitrant states. The MCP is concerned with both microbial uptakes and outputs of DOC compounds, covering a wide range from gene to ecosystem levels. In this minireview, the ATP binding cassette (ABC) transporter is used as an example for the microbial processing of DOC at the genetic level. The compositions of the ABC transporter genes of the two major marine bacterial clades Roseobacter and SAR11 demonstrate that they have distinct patterns in DOC utilization: Roseobacter strains have the advantage of taking up carbohydrate DOC, while SAR11 bacteria prefer nitrogen-containing DOC. At the ecosystem level, bacterially derived RDOC based on D-amino acid biomarkers is reported to be responsible for about a quarter of the total marine RDOC pool. Under future global warming scenarios, partitioning of primary production into DOC could be enhanced, and thus the MCP could play an even more important role in carbon sequestration by the ocean. Joint efforts to study the MCP from multiple disciplines are required to obtain a better understanding of ocean carbon cycle and its coupling with global change.The ocean acts as a "sink" of atmospheric CO 2 , thus mitigating global warming (44, 48). The recognized biological mechanism for this sink is the "biological pump," which is based on the photosynthetic fixation of CO 2 and subsequent carbon export driven mainly by sinking of particulate organic carbon (POC). However, the buried POC in the ocean sediment is Ͻ0.1% of primary production formed in the surface ocean, while the rest of the organic carbon is mainly respired back to CO 2 (14, 28) . Nevertheless, the ocean possesses a huge dissolved organic carbon (DOC) pool, which accounts for about 95% of the total remaining organic carbon (22, 39). The majority of this DOC pool is recalcitrant to biological degradation and can persist in the water column for thousands of years, constituting carbon sequestration in the ocean (4,22,25,39,40). However, the origin of this recalcitrant DOC pool is presently unclear.Recently a new concept was proposed to address this matter, the "microbial carbon pump" (MCP), which refers to the microbial processes that transform labile DOC (LDOC) into recalcitrant DOC (RDOC) (25). The MCP is a conceptual framework to explicitly integrate environmental, trophic, physiological, molecular, and genomic processes relevant to the in situ microbial activities that regulate RDOC production and dynamics (25, 26) (Fig. 1).Diverse microbes and DOC compounds in the ocean. The transformation of DOC is carried out by heterotrophic microbes, and the pathways and rates of DOC transformation determine the ...

Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’

“…For example, ribose, being a lysis product of RNA, is presumably more available in non-oligotrophic environments characterized by higher rates of cell turnover and lysis. Indeed, both the transporters and the carbohydrate utilization patterns of the SAR11 clade comprising the oligotrophic ocean bacteria suggest the inability to takeup and utilize carbohydrates (including ribose) as a carbon and energy source (Jiao and Zheng, 2011). Similarly, PHBs are storage molecules produced by several bacterial species in response to either an excess of carbon or a limitation of another nutrient, ACKGCTCAGTAACACGT ACKGCTCAGTAACACGT A333F TCCAGGCCCTACGGG CCCTAGCCCTAMGGG AB341F CCTACGGGRSGCAGCAG CCTAMGGGRTGCAGCAG A344F ACGGGGTGCAGCAGGCGCGA AMGGGGTGCAGCAGKYRSGA U515F GTGCCAGCMGCCGCGGTAA GTGCCAGCMGCCGCGGTAA U519F CAGCMGCCGCGGTAATWC CAGCMGCCGCGGTAATWC UA571F GCYTAAAGSRICCGTAGC GCYTAAAGSRIYYGTAGC UA751F CCGACGGTGAGRGRYGAA CTGACGGTGAGRRRYGAA AB779F GCRAASSGGATTAGATACCC GCRACSSGGATTAGATACCC EB787F ATTAGATACCCTGGTA ATTAGATACCCGGTTA AB787F ATTAGATACCCGGGTA ATTAGATACCCGGTTA Ab789F TAGATACCCSSGTAGTCC TAGATACCCSSTTAGTCC AB906F GAAACTTAAAKGAATTG GAAACTTAAWKGAATTG A1040F GAGAGGWGGTGCATGGCC GAGAGGWGYTGTATGGYC U1053F GCATGGCYGYCGTCAG GTATGGCYAYYKKCAG A1098F GGCAACGAGCGMGACCC GGCAACGGGCGMGACCY AB127R CCACGTGTTACTSAGC CBACGTGTTACTSAGC A348R CCCCGTAGGGCCYGG CCCCKTAGGGCTAGG U534R GWATTACCGCGGCKGCTG GTATTACCGCGGCGGCTG U529R ACCGCGGCKGCTGGC ACCGCGGCGGCTGGC AB909R TTTCAGYCTTGCGRCCGTAC TTTCACYCTTGCGRGYRTAC A927R CCCGCCAATTCCTTTAAGTTTC CCCGCCAATTCCWTTAAGTTTC A926R CCGTCAATTCCTTTRAGTTT CCGCCAATTCCWTTRAGTTT A934R GTGCTCCCCCGCCAATTCCT GTGMGCYCCCGCCAATTCCW A976R YCCGGCGTTGAMTCCAATT YCYGGCGTTGTRTCCRATT A1115R GGGTCTCGCTCGTTG RGGTCTCGCYCGTTG UA1204R TTMGGGGCATRCIKACCT TTMGGGCYATRCIKAYCT Mismatches in ...…”

Mechanisms of microbial carbon sequestration in the ocean – future research directions

“…A mechanism would be needed to determine a flexible lability continuum according to the nutrient conditions in the overlying epipelagic layer: the continuum would move toward recalcitrance in oligotrophic oceans while being more labile in eutrophic regions (Jiao and Zheng, 2011). Such a model could also include a description of processes in the mesopelagic layer allowing the modification of the accessibility of RDOC to heterotrophic bacteria.…”

“…Roseobacter strains tend to assimilate carbohydrate-rich DOC while SAR11 bacteria prefer nitrogen-containing DOM because they have suites of highaffinity carbohydrate and amino acid ABC transporter systems, respectively (Jiao and Zheng, 2011). Bacteroides and Gammaproteobacteria are able to consume a diverse array of DOC because they have TonB-dependent transporter genes (Tang et al, 2012).…”

Organic Matter and Nutrient Profile of the Two-Current-Regulated-Zone in the Southwestern Sumatran Waters (Ssw)

“…nitrification or denitrification, occur as the phenomena that affects bacteria and phytoplankton (Bianchi et al 1994;Bianchi et al 1995;Ward et al 1989). This has subsequently become known as the phenomena correlated to the biological pump (Herndl & Reinthaler, 2013, Jiao & Zheng, 2011Sanders et al 2014;Tortell et al 1999).…”