Phosphate‐limited ocean regions select for bacterial populations enriched in the carbon–phosphorus lyase pathway for phosphonate degradation

Sosa, Oscar A.; Repeta, Daniel J.; DeLong, Edward F.; Ashkezari, M. D.; Karl, David M.

doi:10.1111/1462-2920.14628

Cited by 99 publications

(137 citation statements)

References 72 publications

Supporting

Mentioning

119

Contrasting

Order By: Relevance

“…3c). These results show that the oligotrophic seawater in the SCS has strong positive feedback to the added MPn, thereby supporting the presence of MPn-dependent CH 4 production, and its contribution to the methane paradox likely depends on the inventory of organic matter with C P bonds (Sosa et al 2019).…”

Section: Mpn-dependent Ch 4 Production In the Eutrophic Yellow Seasupporting

confidence: 59%

Methane production in oxic seawater of the western North Pacific and its marginal seas

Wang

Zhang

et al. 2020

Limnology & Oceanography

View full text Add to dashboard Cite

The oceans are natural sources of atmospheric methane (CH 4), but the origin of excess CH 4 at the surface remains enigmatic. Incubation experiments were conducted in the western North Pacific (WNP) and its marginal seas (i.e., Yellow Sea and South China Sea [SCS]) to identify the degradation of methylphosphonate (MPn) to CH 4 in the oceans and the microbes associated with MPn-driven CH 4 production. In the coastal seawater of the Yellow Sea, CH 4 was observed to accumulate after MPn enrichment with a high MPn to CH 4 conversion efficiency (approximately 60%). Dissolved inorganic phosphorus (Pi) did not effectively restrict the microbial utilization of MPn in the eutrophic coastal waters. The results of 16S rRNA gene sequencing showed that Vibrio spp. were the dominant bacteria in the MPn-amended treatments. Moreover, several Vibrio isolates isolated from the coastal waters were found to produce CH 4 while growing in culture using MPn as the sole P source, thereby indicating that Vibrio spp. might be the major contributors to MPn-dependent CH 4 production. In oligotrophic areas, such as the SCS and WNP, CH 4 production from MPn metabolism was also observed in the surface seawater. In contrast to coastal waters, this pathway in oligotrophic areas is regulated by dissolved Pi availability. This work confirms that aerobic CH 4 formation from MPn degradation can occur both in eutrophic coastal waters and oligotrophic oceans driven by MPn-utilizing microorganisms (especially heterotrophic bacteria), which may have a significant impact on our understanding of the CH 4 and P cycles in global oceans. Methane (CH 4) is a greenhouse gas that plays an important role in global warming. Oceans are a natural source of atmospheric CH 4 and contribute 1-4% of the annual global emissions (IPCC 2013). Studies have shown that the oxygenated surface waters throughout the majority of the global oceans are supersaturated with CH 4 with respect to the atmosphere, thereby implying a local CH 4 source. However, the origin of oceanic surface CH 4 is not sufficiently understood (Reeburgh 2007). Traditional CH 4 production is thought to be a strictly anaerobic process mediated by methanogenic archaea, which are outperformed by sulfate-reducing bacteria when competing for potential substrates (such as H 2 and acetate) (Sorokin et al. 2017). Methanogenesis appears to be inhibited by the presence of well-mixed oxygen and sulfate in the ocean surface. However, recent studies have shown that methylated compounds, such as

show abstract

Section: Mpn-dependent Ch 4 Production In the Eutrophic Yellow Seasupporting

confidence: 59%

Methane production in oxic seawater of the western North Pacific and its marginal seas

Wang

Zhang

et al. 2020

Limnology & Oceanography

View full text Add to dashboard Cite

show abstract

“…If we account for bulk organic‐C from Station ALOHA surface waters (δ 13 C VPDB = −22‰; Repeta et al, ), microbially produced MPn (and resultant methane) is offset from bulk organic matter by nearly −20‰: that is, [−22‰ (C org )] + [−20‰ (offset)] ≅ [−43‰ (CH 4 _average)] ≅ [MPn + 1.3‰]. If MPn producers reflect the depth distributions of the heterotrophic SAR11‐type bacteria and bicarbonate‐fixing AOAs (Carlson et al, ; Newell et al, ; Sosa et al, ), then heterotrophic bacteria are the more abundant microbes in surface waters (>350m) at Station ALOHA, where the concentrations of methane were highest, and carbon isotope delta values were the most depleted. At depth (<350 m), AOAs were numerically dominant (DeLong et al, ; Santoro et al, ; Schattenhofer et al, ), though dissolved methane concentrations decreased with a concomitant rise in carbon isotope values (δ 13 C VPDB range of −10 to −30‰; Figures a and c).…”

Section: Resultsmentioning

confidence: 99%

“…Under the panels are the fractionation factors by either the C-P lyase or the major anaerobic (acetate-or CO 2 -dependent) pathways, then applied to bulk organic C-isotope values from Station ALOHA. Values in panels a and c are compiled fromHolmes et al (2000) andSasakawa et al (2008), and for B are fromSosa et al (2019). The fractionation factors are fromFigure 2.…”

mentioning

confidence: 99%

Microbial Methane From Methylphosphonate Isotopically Records Source

Taenzer

Carini

Masterson

et al. 2020

Geophysical Research Letters

View full text Add to dashboard Cite

Methane is a potent greenhouse gas commonly supersaturated in the oxic surfaces waters of oceans and lakes, yet canonical microbial methanogens are obligate anaerobes. One proposed methane production pathway involves microbial degradation of methylphosphonate (MPn), which can proceed in the presence of oxygen. Directly tracing dissolved methane to its source in oxic waters, however, remains a challenge. To address this knowledge gap, we quantified the carbon isotopic fractionation between substrate MPn and product methane (1.3‰) in lab experiments, which was 1 to 2 orders of magnitude smaller than canonical pathways of microbial methanogenesis (20 to 100‰). Together, these results indicated that microbial catabolism of MPn is a source of methane in surface oceans and lake waters, but to differentiate sources of MPn in nature a further accounting of all sources is necessary. Methane from this pathway must be considered in constraining the marine carbon cycle and methane budget.

show abstract

“…The phosphonates might originate from the fungal on October 2, 2020 by guest http://aem.asm.org/ Downloaded from hyphae since phosphonates are reported to be components of fungal exopolysaccharides, glycoproteins and membrane phosphonolipids (42). Phosphonates are very stable organic phosphates, and bacterial phosphonate utilization has been reported in particular in phosphate-limited marine waters where the carbon-phosphorus lyase pathway for phosphonate degradation is enriched (43). It can therefore be speculated that the high relative abundance of phnK in most hyphosphere communities may reflect limitation of easily available P.…”

Section: Effects Of Fertilizer Regime On Bacteria Community Potentialmentioning

confidence: 99%

Different Effects of Soil Fertilization on Bacterial Community Composition in the Penicillium canescens Hyphosphere and in Bulk Soil

Zhang

Hao

García-Lemos

et al. 2020

Appl Environ Microbiol

View full text Add to dashboard Cite

This study investigated the effects of long-term soil fertilization on the composition and potential for phosphorus (P) and nitrogen (N) cycling of bacterial communities associated with hyphae of the P-solubilizing fungus Penicillium canescens. Using a baiting approach, hyphosphere bacterial communities were recovered from three soils that had received long-term amendment in the field with mineral or mineral plus organic fertilizers. P. canescens hyphae recruited bacterial communities with a decreased diversity and an increased abundance of Proteobacteria relative to what was observed in soil communities. As core bacterial taxa, Delftia and Pseudomonas spp. were present in all hyphosphere samples irrespective of soil fertilization. However, the type of fertilization showed significant impacts on the diversity, composition, and distinctive taxa/operational taxonomic units (OTUs) of hyphosphere communities. The soil factors P (Olsen method), exchangeable Mg, exchangeable K, and pH were important for shaping soil and hyphosphere bacterial community compositions. An increased relative abundance of organic P metabolism genes was found in hyphosphere communities from soil that had not received P fertilizers, which could indicate P limitation near the fungal hyphae. Additionally, P. canescens hyphae recruited bacterial communities with a higher abundance of N fixation genes than found in soil communities, which might imply a role of hyphosphere communities for fungal N nutrition. Furthermore, the relative abundances of denitrification genes were greater in several hyphosphere communities, indicating an at least partly anoxic microenvironment with a high carbon-to-N ratio around the hyphae. In conclusion, soil fertilization legacy shapes P. canescens hyphosphere microbiomes and their functional potential related to P and N cycling. IMPORTANCE P-solubilizing Penicillium strains are introduced as biofertilizers to agricultural soils to improve plant P nutrition. Currently, little is known about the ecology of these biofertilizers, including their interactions with other soil microorganisms. This study shows that communities dominated by Betaproteobacteria and Gammaproteobacteria colonize P. canescens hyphae in soil and that the compositions of these communities depend on the soil conditions. The potential of these communities for N and organic P cycling is generally higher than that of soil communities. The high potential for organic P metabolism might complement the ability of the fungus to solubilize inorganic P, and it points to the hyphosphere as a hot spot for P metabolism. Furthermore, the high potential for N fixation could indicate that P. canescens recruits bacteria that are able to improve its N nutrition. Hence, this community study identifies functional groups relevant for the future optimization of next-generation biofertilizer consortia for applications in soil.

show abstract

Phosphate‐limited ocean regions select for bacterial populations enriched in the carbon–phosphorus lyase pathway for phosphonate degradation

Cited by 99 publications

References 72 publications

Methane production in oxic seawater of the western North Pacific and its marginal seas

Methane production in oxic seawater of the western North Pacific and its marginal seas

Microbial Methane From Methylphosphonate Isotopically Records Source

Different Effects of Soil Fertilization on Bacterial Community Composition in the Penicillium canescens Hyphosphere and in Bulk Soil

Contact Info

Product

Resources

About