The persisting textbook notion that oxygenic photosynthesis is mainly driven by visible wavelengths of light (400–700 nm) and chlorophyll (Chl) a as the major photopigment is challenged; recent findings indicate that cyanobacteria with red-shifted chlorophylls and phycobiliproteins capable of harvesting near-infrared-radiation (NIR) at wavelengths > 700–760 nm and exhibiting a pronounced plasticity in their photoacclimatory responses (Gan et al., 2014; Gan and Bryant, 2015) are widespread in natural habitats (Gan et al., 2015; Zhang et al., 2019; Behrendt et al., 2019). Besides the Chl d-containing cyanobacterium Acaryochloris marina, which was originally isolated from tropical ascidians (Miyashita, 2014) but has now been found in many other habitats (Behrendt et al., 2011; Zhang et al., 2019), the discovery of Chl f (Chen et al., 2010) and its occurrence in many different cyanobacteria (Gan et al., 2015) has triggered a substantial amount of research on the biochemistry and molecular physiology of Chl f-containing cyanobacterial strains (Airs et al., 2014; Allakhverdiev et al., 2016; Chen, 2014; Ho et al., 2016; Nürnberg et al., 2018). In comparison, the in situ distribution and activity of Chl f-containing cyanobacteria and their role in primary productivity remain largely unexplored. Here, we used a novel combination of hyperspectral imaging, confocal laser scanning microscopy, and chemical imaging of O₂ for high-resolution mapping of the distribution of Chl f–containing cyanobacteria and their NIR-driven oxygenic photosynthesis in an intertidal beachrock habitat. Our study gives novel insight into the ecological niche and importance of endolithic Chl f-containing cyanobacteria, and indicates that high rates of NIR-driven oxygenic photosynthesis can contribute to primary production in natural biofilm habitats.

With an in vivo absorption range of 700–760 nm, Chl f is the most red-shifted chlorophyll, which was first found in the filamentous cyanobacterium Halomicronema hongdechloris isolated from stromatolites in Western Australia (Chen et al., 2010; Chen et al., 2012), and in an unicellular cyanobacterium (strain KC1 related to Aphanocapsa spp.) isolated from Lake Biwa, Japan (Akutsu et al., 2011). However, Bryant and coworkers discovered that the ability to synthesize Chl f, far-red shifted phycobiliproteins, and small amounts of Chl d can be induced in many different cyanobacteria, including representatives from all five major subdivisons, when grown under far-red light-enriched conditions (Gan et al., 2014; Gan et al., 2015). Such far-red light photoacclimation (FaRLiP) involves remodeling of the photosynthetic apparatus via synthesis and modification of pigments and pigment-protein complexes. This remodeling is primarily regulated at the transcriptional level via upregulation of paralogous photosynthesis-related genes in a 21-gene cluster, which seems largely conserved in cyanobacteria exhibiting FaRLiP (Gan and Bryant, 2015) and contains genes for a red phytochrome-triggered control cascade of FaRLiP (Zhao et al., 2015). Recently, it was shown that FaRLiP also involves the modification and inclusion of Chl f in both PSI and PSII (Itoh et al., 2015; Nürnberg et al., 2018).

Besides their strong relevance for exploring the biophysical and biochemical limits and controls of oxygenic photosynthesis, cyanobacteria with Chl d and Chl f have been employed in speculations on more efficient light harvesting of solar energy, as organisms with red-shifted photopigments can in principle exploit ~20% more photons in the solar spectrum for their photosynthesis (Chen and Blankenship, 2011). However, FaRLiP involves remodeling of the photosynthetic apparatus for better performance under 700–760 nm light and is apparently not induced in absence of NIR (Gan et al., 2014), and Acaryochloris marina has largely exchanged its Chl a with Chl d (Miyashita, 2014). Hence, the selective benefit of employing Chl d, Chl f, and red-shifted phycobiliproteins in oxygenic photosynthesis may be more related to the capability of exploring special ecological niches in the shadow of other oxygenic phototrophs (Ohkubo and Miyashita, 2017; Kühl et al., 2005). But we know nothing about the quantitative role of cyanobacteria with far red-shifted photopigments for primary production in natural habitats.

There is a growing database of cyanobacteria and habitats wherein Chl f has been detected (Supplementary file 1). However, only three studies have reported on the actual distribution and niche of Chl f-containing cyanobacteria in their natural habitats (Trampe and Kühl, 2016; Ohkubo and Miyashita, 2017; Behrendt et al., 2019), and hitherto NIR-driven oxygenic photosynthesis by Chl f-containing cyanobacteria has not been demonstrated in situ. This is experimentally challenging, as cyanobacteria exhibiting FaRLiP respond to the local light microenvironment and typically occur in dense proximity with other oxygenic phototrophs harboring a plethora of photopigments fueling Chl a-based oxygenic photosynthesis by visible light (400–700 nm) (Ohkubo and Miyashita, 2017; Behrendt et al., 2015). Consequently, photosynthetic activity of Chl f-containing cyanobacteria has only been measured on strains (e.g. Gan et al., 2014; Nürnberg et al., 2018) or enrichments isolated from their natural habitat (e.g. Behrendt et al., 2015). Detailed microscopic investigation of pigmentation in cyanobacteria with Chl f has also largely been limited to culture material (Majumder et al., 2017; Zhang et al., 2019).

Beachrock is a widespread sedimentary rock formation on (sub)tropical, intertidal shorelines, where a mixture of biogeochemical processes cement carbonate sands together into a porous solid matrix (Vousdoukas et al., 2007). The upper surface of light-exposed beachrock is colonized by dense microbial biofilms dominated by cyanobacteria (Cribb, 1966; Díez et al., 2007), which are embedded in a dense exopolymeric matrix covering the surface and endolithic pore space of the beachrock (Petrou et al., 2014). We previously demonstrated the presence of Chl f-containing cyanobacteria in an endolithic niche below the surface biofilm along with the ability of beachrock samples to upregulate their Chl f-content upon incubation under NIR, indicative of FaRLiP (Trampe and Kühl, 2016). Here, we correlate the spatial organization of Chl f-containing cyanobacteria with direct in vivo measurements of their NIR-driven O₂ production in a natural beachrock habitat.

Hyperspectral reflectance imaging on vertical cross-sections of beachrock submerged in seawater (23°C and salinity = 35) revealed the presence of a dense ~1 mm thick surface biofilm with high amounts of Chl a, while a more patchy zone containing Chl f, and less Chl a was found below the surface biofilm of the beachrock (Figure 1A,B), exhibiting localized hot spots of Chl f concentration (Figure 1C). Representative reflectance spectra from these regions carrying spectral signatures of maximal Chl a and Chl f absorption at 670–680 nm and 715–725 nm, respectively, are presented in the Supplementary Materials (Figure 1—figure supplement 1) along with additional examples of hyperspectral imaging of beachrock cross-sections (Figure 1—figure supplement 2). The presence of Chl f (and absence of microalgal Chl b and c) in our samples was confirmed by HPLC analysis of beachrock pigment extracts (see Materials and methods), both in a ~ 0–2 mm thick black beachrock sample, and in a more distinct green endolithic layer (~2–5 mm below the beachrock surface) (Figure 1—figure supplement 3). The amount of Chl f relative to Chl a in these samples ranged from 3.5% in the mixed layer to 6% in the green layer, while Trampe and Kühl (2016) reported Chl f amounts ranging from 0.5% to 5% of Chl a in beachrock.

Figure 1 with 8 supplements see all

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To further describe the microscale distribution of cells with different photo-pigmentation, we employed hyperspectral fluorescence imaging with confocal laser scanning microscopy (CLSM; 488 nm excitation) on beachrock cross-sections (Figure 1—figure supplements 4 and 5). The CLSM data confirmed the occurrence of patches of filamentous and unicellular Chl f-containing cyanobacteria with a characteristic fluorescence peak around 740–750 nm (cf. Majumder et al., 2017) in deeper endolithic zones (Figure 1—figure supplements 4C and 5A–D). Besides filamentous morphotypes, brightfield microscopy of Chl f hot spots revealed the presence of larger round cell aggregates (Figure 1—figure supplement 5E,F) typical of pleurocapsalean cyanobacteria (Waterbury and Stanier, 1978).

In order to confirm the apparent dominance of cyanobacteria over microalgal oxygenic phototrophs, we employed 16S rRNA gene amplicon sequencing on black beachrock samples taken from the same area as the samples used for hyperspectral and O₂ imaging. Among ~39,000 cyanobacterial-like sequences obtained from the black beachrock, none were classified as chloroplasts. In contrast, among ~17,000 cyanobacterial-like sequences obtained from two samples of seawater, 18% were classified as chloroplasts (Supplementary file 2). Microalgae are thus likely to be completely absent from the black beachrock, where the oxygenic phototrophic community consists exclusively of cyanobacteria.

Analysis of a distinct green layer below the black beachrock surface biofilm showed that most cyanobacterial OTU’s were clustering with Halomicronema (harboring the Chl f-containing species Halomicronema hongdechloris; Chen et al., 2012) as well as coccoid Pseudocapsa and Chroococcidiopsis (Supplementary file 2). The surface layer of the black beachrock harbored a higher cyanobacterial diversity with most OTU’s clustering with Rivularia, Calothrix, and Halomicronema, as well as numerous smaller populations clustering with Chroococcidiopsis and other coccoid cyanobacteria. These data confirm earlier findings of i) Chl f (and only minor amounts of Chl d) in beachrock (Trampe and Kühl, 2016), and ii) a predominance of cyanobacteria as the major oxygenic phototrophs in beachrock (Cribb, 1966; Díez et al., 2007). We note that a comprehensive description of the cyanobacterial diversity associated with beachrock was beyond the scope of the present study, and a detailed study of the microbial diversity in beachrock (based on 16S rRNA amplicon and metagenomic sequencing) will be presented elsewhere. Here, we focus on the photosynthetic activity of Chl f-containing cyanobacteria in beachrock.

By coating beachrock cross-sections with a thin (<1 mm) layer of an O₂-sensitive nanoparticle-agarose paint (see Materials and methods and Figure 1—figure supplement 6) and subsequent immersion in anoxic water, it was possible to map the local O₂ production over the beachrock cross-section when illuminated with weak NIR levels (740 nm, 25 nm half bandwidth; 28 µmol photons m⁻² s⁻¹). We observed hot spots of NIR-driven photosynthesis driving local O₂ levels from 0% to >40–50% air saturation within 15–20 min (Figure 1D, Figure 1—figure supplement 7), which overlapped with regions of high Chl f absorption (Figure 1C, Figure 1—figure supplement 3). The build-up of O₂ in the hotspots harboring Chl f occurred rapidly after onset of NIR illumination and dissipated rapidly back to anoxia within a few minutes after darkening (see Video 1). Based on O₂ concentration images recorded at 5 min intervals after experimental light-dark shifts, we calculated images of apparent dark respiration and NIR-driven net and gross photosynthesis that could be mapped onto the beachrock structure (Figure 2A–D) showing that hotspots of activity aligned with the presence of Chl f (see Figure 1B,C). We extracted estimates of maximum O₂ conversion rates in particular regions of interest (ROI) showing high rates of NIR-driven gross photosynthesis of ~5–15 µmol O₂ L⁻¹ min⁻¹ in the beachrock under the given actinic irradiance of 28 µmol photons m⁻² s⁻¹; a similar range was found for two other beachrock cross-sections (data not shown). These volume-specific rates fall among the upper range of maximal gross photosynthesis rates in aquatic phototrophs, and are comparable with photosynthetic rates found in benthic microalgae (Krause-Jensen and Sand-Jensen, 1998).

Figure 2

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Video 1

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The Chl f-driven oxygenic photosynthesis by endolithic cyanobacteria thus seems very efficient given the low actinic NIR level applied. High photosynthetic efficiency of Chl f-containing cyanobacteria under NIR has been shown in previous ex situ studies on cultivated strains and enrichments. Gan et al. (2014) thus found that Leptolyngbya strain JSC-1 cells showed a 40% higher O₂ production rate with NIR after undergoing FaRLiP relative to cells grown under red light (Gan et al., 2014), and a similar high photosynthetic efficiency was found in a Chroococcidiopsis strain (Nürnberg et al., 2018). Using similar NIR levels as used in the present study, Behrendt et al. (2015) showed rapid saturation of NIR-driven oxygenic photosynthesis already at 25–30 µmol photons m⁻² s⁻¹ (740 nm) in a cell enrichment with Chl f-containing, Aphanocapsa-like cyanobacteria from a cavernous biofilm.

Our structural and chemical imaging of beachrock showed that Chl f and NIR-driven O₂ production was confined to a relative narrow zone 1–2 mm below the beachrock surface in the investigated samples (Figure 1, Figure 2; Figure 1—figure supplements 2, 4 and 5). Assuming a NIR-driven oxygenic photosynthesis rate of 10 µmol O₂ L⁻¹ min⁻¹ (=nmol O₂ cm⁻³ beachrock min⁻¹) in a 1 mm thick layer (Figure 2), and a conservative estimate of beachrock porosity of ~0.4 in the uppermost 1–2 mm (Vousdoukas et al., 2007), we can estimate the areal NIR-driven gross photosynthesis rate to (10 µmol L⁻¹ min⁻¹ × 0.4×0.1 cm x 10⁻⁶ x 10000 x 60 =) ~0.24 mmol O₂ m⁻² beachrock h⁻¹. Total beachrock primary productivity remains to be quantified in detail, but it is well known that beachrock habitats sustain high grazing rates of epifauna (McLean, 1974; McLean, 2011) and herbivorous reef fish (Stephenson and Searles, 1960).

To our knowledge, beachrock primary production has only been reported by Krumbein, who studied a Red Sea beachrock habitat (Krumbein, 1979). Based on his data on O₂ exchange under water covered conditions (cf. Figure 13 in Krumbein, 1979), we estimated a total gross photosynthesis of ~10 mmol O₂ m⁻² beachrock h⁻¹. While based on several crude assumptions and comparing different habitats, these rough calculations indicate that NIR-driven photosynthesis could account for at least 2–3% of total areal photosynthesis in beachrock habitats. Furthermore, we note that we base this estimate on O₂ dynamics over minutes measured in a thin agar layer adjacent to the actual phototrophic cells, which will underestimate the true dynamics (see Materials and methods), and our measurements were conducted at low NIR levels that may not represent saturated photosynthesis rates. Obviously, the realized total daily primary productivity will also be strongly modulated by the actual biomass distribution, porosity and diel light exposure within the beachrock, as well as the pronounced diel cycles of environmental conditions on the beachrock platform (Petrou et al., 2014; Schreiber et al., 2002). Nevertheless, we argue that our experimental data point to a significant role of NIR-driven oxygenic photosynthesis in beachrock and potentially other endolithic habitats.

Based on the origin of isolates shown to employ FaRLiP (Supplementary file 1), it has been speculated that shaded soils, caves, plant canopies and thermal springs may be prime terrestrial habitats for cyanobacteria with Chl f (Gan et al., 2015; Zhang et al., 2019). Beachrock is widespread in intertidal zones on a global scale (Vousdoukas et al., 2007) and our study shows that these habitats may present a major ecological niche for cyanobacteria with FaRLiP and NIR-driven oxygenic photosynthesis in marine intertidal habitats. While we present the hitherto most detailed insight into the distribution and in situ activity of Chl f-containing cyanobacteria in intact samples from a natural habitat, there is now a need for more precise characterization of the microenvironment and metabolic activities of microorganisms in beachrock to assess the quantitative importance of NIR-driven oxygenic photosynthesis for system productivity.

The present study and the few other studies of natural habitats (Supplementary file 1) demonstrate that a key trait of such cyanobacteria is the formation of biofilms in strongly shaded environments below other algae, cyanobacteria or terrestrial plants, or in the twilight zone of caves (Behrendt et al., 2019). It remains to be explored to what extent the presence of cyanobacteria with FaRLiP-capability or constitutive high Chl d levels play a role for overall photosynthetic productivity in such habitats. That is, does the complementary photopigmentation of cyanobacteria with far-red shifted photopigments in the ‘understory’ of other oxygenic phototrophs lead to higher photosynthetic efficiency and productivity at the community/system level, for example in analogy to plant canopies? Such studies are complicated due to the compacted and often stratified structure of the natural communities, but the novel combination of structural and chemical imaging presented here seems a promising toolset for unraveling the ecological importance of FaRLiP and cyanobacteria with far red-shifted photopigments.

All data generated or analysed during this study are included in the manuscript and supporting files.

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Author details

1. Michael Kühl

   1. Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark
   2. Climate Change Cluster, University of Technology Sydney, Sydney, Australia

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Project administration, Writing, Original draft, Review and editing

   For correspondence

   mkuhl@bio.ku.dk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1792-4790

2. Erik Trampe

   Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark

   Contribution

   Conceptualization, Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3249-0297

3. Maria Mosshammer

   Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark

   Contribution

   Investigation, Methodology, Review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7296-8673

4. Michael Johnson

   iThree Institute, University of Technology Sydney, Sydney, Australia

   Contribution

   Resources, Software, Formal analysis, Investigation, Visualization, Methodology, Review and editing

   Competing interests

   No competing interests declared

5. Anthony WD Larkum

   Climate Change Cluster, University of Technology Sydney, Sydney, Australia

   Contribution

   Investigation, Visualization, Methodology, Review and editing

   Competing interests

   No competing interests declared

6. Niels-Ulrik Frigaard

   Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark

   Contribution

   Conceptualisation, Resources, Data curation, Formal analysis, Validation, Investigation, Methodology, Review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9389-8109

7. Klaus Koren

   1. Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark
   2. Centre for Water Technology, Section for Microbiology, Department of Bioscience, University of Aarhus, Aarhus, Denmark

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7537-3114

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