Prosthecochloris marina sp. nov., a new green sulfur bacterium from the coastal zone of the South China Sea

19Endolithic microbial symbionts in the coral skeleton may play a pivotal role in 20 maintaining coral health. However, compared to aerobic microorganisms, research on the 21 roles of endolithic anaerobic microorganisms and microbe-microbe interactions in the coral 22 skeleton are still in their infancy. In our previous study, we showed that a group of coral-23 associated Prosthecochloris (CAP), a genus of anaerobic green sulfur bacteria, was 24 dominant in the skeleton of the coral Isopora palifera. Though CAP is diverse, the 16S 25 rRNA phylogeny presents it as a distinct clade separate from other free-living 26Prosthecochloris. In this study, we build on previous research and further characterize the 27 genomic and metabolic traits of CAP by recovering two new near-complete CAP 28 genomes-Candidatus Prosthecochloris isoporaea and Candidatus Prosthecochloris sp. 29 N1-from coral Isopora palifera endolithic cultures. Genomic analysis revealed that these 30 two CAP genomes have high genomic similarities compared with other Prosthecochloris 31 and harbor several CAP-unique genes. Interestingly, different CAP species harbor various 32 pigment synthesis and sulfur metabolism genes, indicating that individual CAPs can adapt 33 to a diversity of coral microenvironments. A novel near-complete SRB genome-34Candidatus Halodesulfovibrio lyudaonia-was also recovered from the same culture. The 35 fact that CAP and various sulfate-reducing bacteria (SRB) co-exist in coral endolithic 36 cultures and coral skeleton highlights the importance of SRB in the coral endolithic 37 community. Based on functional genomic analysis of Ca. P. sp. N1 and Ca. H. lyudaonia, 38 we also propose a syntrophic relationship between the SRB and CAP in the coral skeleton. 39 40 Importance 41Little is known about the ecological roles of endolithic microbes in the coral skeleton; 42 one potential role is as a nutrient source for their coral hosts. Here, we identified a close 43 ecological relationship between CAP and SRB. Recovering novel near-complete CAP and 44 SRB genomes from endolithic cultures in this study enabled us to understand the genomic 45 and metabolic features of anaerobic endolithic bacteria in coral skeletons. These results 46 demonstrate that CAP members with similar functions in carbon, sulfur, and nitrogen 47 metabolisms harbor different light-harvesting components, suggesting that CAP in the 48 skeleton adapts to niches with different light intensities. Our study highlights the potential 49 ecological roles of CAP and SRB in coral skeletons and paves the way for future 50 investigations into how coral endolithic communities will respond to environmental 51 changes. 52 53 54 55

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“…N1. Its genome size was 2.7 Mb, with 23 contigs and a 47.0% GC ratio, which is consistent with the genome of Prosthecochloris marina V1 (23).…”

Section: Resultssupporting

confidence: 73%

A genomic view of coral-associatedProsthecochlorisand a companion sulfate-reducing bacterium

Chen

Yang

Tandon

et al. 2019

Preprint

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“…A number of organisms containing oxidative-type dissimilatory sulfite reductase feature an DsrL-2 enzyme reacting exclusively with NADP(H) (Figure 2). Two of the respective organisms are very well-established sulfur oxidizers (Imhoff and Thiel, 2010;Bryantseva et al, 2019). We conclude that in this case NADP + is the electron acceptor for rDsrABL-2-catalyzed sulfite formation and that all organisms containing the rDsrABL-2 combination have the potential for sulfur oxidation.…”

Section: Discussionmentioning

confidence: 78%

“…The second large DsrL group (DsrL-2) comprises proteins from two green sulfur bacteria, Chlorobium phaeobacteroides and Prosthecochloris marina V1 that are established sulfur oxidizers (Imhoff, 2014;Bryantseva et al, 2019). These sequence are located on the same major branch as DsrL-2 proteins assigned to members of the Nitrospirae, one Nitrospinae bacterium, Actinobacteria (Gaiellales bacterium SURF_19) and several Deltaproteobacteria including strains of the genera Desulfopila and Desulforhopalus.…”

Section: Correlation Of Dsrl and Dsra Phylogeniesmentioning

confidence: 99%

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The Iron-Sulfur Flavoprotein DsrL as NAD(P)H:Acceptor Oxidoreductase in Oxidative and Reductive Dissimilatory Sulfur Metabolism

et al. 2020

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DsrAB-type dissimilatory sulfite reductase is a key enzyme of microbial sulfurdependent energy metabolism. Sulfur oxidizers also contain DsrL, which is essential for sulfur oxidation in Allochromatium vinosum. This NAD(P)H oxidoreductase acts as physiological partner of oxidative-type rDsrAB. Recent analyses uncovered that DsrL is not confined to sulfur oxidizers but also occurs in (probable) sulfate/sulfur-reducing bacteria. Here, phylogenetic analysis revealed a separation into two major branches, DsrL-1, with two subgroups, and DsrL-2. When present in organisms with reductivetype DsrAB, DsrL is of type 2. In the majority of cases oxidative-type rDsrAB occurs with DsrL-1 but combination with DsrL-2-type enzymes is also observed. Three model DsrL proteins, DsrL-1A and DsrL-1B from the sulfur oxidizers A. vinosum and Chlorobaculum tepidum, respectively, as well as DsrL-2 from thiosulfate-and sulfur-reducing Desulfurella amilsii were kinetically characterized. DaDsrL-2 is active with NADP(H) but not with NAD(H) which we relate to a conserved YRR-motif in the substrate-binding domains of all DsrL-2 enzymes. In contrast, AvDsrL-1A has a strong preference for NAD(H) and the CtDsrL-1B enzyme is completely inactive with NADP(H). Thus, NAD + as well as NADP + are suitable in vivo electron acceptors for rDsrABL-1-catalyzed sulfur oxidation, while NADPH is required as electron donor for sulfite reduction. This observation can be related to the lower redox potential of the NADPH/NADP + than the NADH/NAD + couple under physiological conditions. Organisms with a rdsrAB and dsrL-1 gene combination can be confidently identified as sulfur oxidizers while predictions for organisms with other combinations require much more caution and additional information sources.

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“…The results of the GTDB-Tk taxonomy assignment showed that all Prosthecochloris -related bins were closest to Prosthecochloris marina V1, which was identified from steel plates in the coastal zone of the South China Sea in 2019 [50]. Interestingly, Prosthecochloris -related bins in N2 and N3 shared only 90 % ANI with Prosthecochloris marina V1 (), which is below the 95 % ANI cutoff, a frequently used standard for species delineation [51].…”

Section: Resultsmentioning

confidence: 99%

Potential syntrophic relationship between coral-associated Prosthecochloris and its companion sulfate-reducing bacterium unveiled by genomic analysis

et al. 2021

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Endolithic microbial symbionts in the coral skeleton may play a pivotal role in maintaining coral health. However, compared to aerobic micro-organisms, research on the roles of endolithic anaerobic micro-organisms and microbe–microbe interactions in the coral skeleton are still in their infancy. In our previous study, we showed that a group of coral-associated Prosthecochloris (CAP), a genus of anaerobic green sulphur bacteria, was dominant in the skeleton of the coral Isopora palifera. Though CAP is diverse, the 16S rRNA phylogeny presents it as a distinct clade separate from other free-living Prosthecochloris . In this study, we build on previous research and further characterize the genomic and metabolic traits of CAP by recovering two new high-quality CAP genomes – Candidatus Prosthecochloris isoporae and Candidatus Prosthecochloris sp. N1 – from the coral I. palifera endolithic cultures. Genomic analysis revealed that these two CAP genomes have high genomic similarities compared with other Prosthecochloris and harbour several CAP-unique genes. Interestingly, different CAP species harbour various pigment synthesis and sulphur metabolism genes, indicating that individual CAPs can adapt to a diversity of coral microenvironments. A novel high-quality genome of sulfate-reducing bacterium (SRB)– Candidatus Halodesulfovibrio lyudaonia – was also recovered from the same culture. The fact that CAP and various SRB co-exist in coral endolithic cultures and coral skeleton highlights the importance of SRB in the coral endolithic community. Based on functional genomic analysis of Ca. P. sp. N1, Ca. P. isoporae and Ca. H. lyudaonia, we also propose a syntrophic relationship between the SRB and CAP in the coral skeleton.

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Prosthecochloris marina sp. nov., a new green sulfur bacterium from the coastal zone of the South China Sea

Cited by 12 publications

References 19 publications

A genomic view of coral-associatedProsthecochlorisand a companion sulfate-reducing bacterium

A genomic view of coral-associatedProsthecochlorisand a companion sulfate-reducing bacterium

The Iron-Sulfur Flavoprotein DsrL as NAD(P)H:Acceptor Oxidoreductase in Oxidative and Reductive Dissimilatory Sulfur Metabolism

Potential syntrophic relationship between coral-associated Prosthecochloris and its companion sulfate-reducing bacterium unveiled by genomic analysis

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