Geobiology (2009),

7

, 97–99 DOI: 10.1111/j.1472-4669.2009.00196.x

© 2009 The AuthorJournal compilation © 2009 Blackwell Publishing Ltd

97

Blackwell Publishing LtdOxford, UKGBIGeobiology1472-46771472-4669Blackwell Publishing Ltd 2009XXXEditorialCoevolution of photosynthetic organisms and the environmentEditorial

Introduction to Special Issue

Coevolution of photosynthetic organisms and the environment

D. J . BEERLING

Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

INTRODUCTION

Geobiology has been broadly defined (although not by thisjournal) as the investigation of the influence of biology on thephysical features of the Earth system, including its climatic,atmospheric, oceanic and geospheric components. But thisdefinition is limited, it captures only one half of the story.Changes in the operation of the Earth system also feedbackto influence biology, with the capacity to alter the course ofits evolutionary trajectories (Beerling, 2007).

Building a better understanding of the dynamic behaviourof Earth’s coupled biological and physical systems, then, is theformidable task facing geobiologists. It requires investigationsbridging across different disciplines ranging from microbiology,physiology, geochemistry, mineralogy and palaeontology.It further demands approaches encompassing process-basedmodels, as well as the collection of empirical evidence obtainedfrom the sedimentary and rock records, controlled environ-ment studies and field investigations.

Knoll (2003) rightly drew attention to the early evolutionand spread of oxygenic photosynthetic organisms around2.5 billion years ago as a classic example demonstrating thecoevolution of biology and the Earth’s geochemical systems.But intensive research over the intervening time has widenedthe scope of the interactions between photosynthetic organismsand the environment. Consequently, terrestrial and marinephotosynthetic ecosystems are increasingly being recognizedas geological forces of nature, moulding both climate andatmospheric composition on long and short timescales(Beerling

et

al

., 2007; Beerling, 2007; Falkowski & Knoll,2007).

The collection of papers in this Special Issue showcases aselection of new findings, and signposts exciting new directionsin geobiological research. It illustrates how the emerging debateis broadening by revealing the diversity of environmentalinteractions photosynthetic organisms participate in, and areinfluenced by. It also reveals the wide diversity of techniquesand approaches being used to investigate and uncover thecomplex nature of such interactions.

COEVOLUTION IN THE OCEANS

In the oceans, Glass

et

al

. integrate geochemical, palaeonto-logical, and biochemical evidence to infer changes in theuse of metals for N assimilation by marine primary pro-ducers over geological time. Drawing evidence from thesedifferent sources, the authors propose a novel hypothesisfor changes in the availability of metals (Fe, Mo) in relationto the oxidation state of the oceans driving their usage inmetalloenzyme systems metabolizing N. They provide astrong case for environmental influence on the evolutionof metal requirements that has the attraction of gene-rating testable hypotheses, an important feature of whatgeobiology should be about. As the authors propose, theirhypotheses can be evaluated by investigating the metalrequirements in N metabolism of different groups of marineorganisms.

Dealing with aquatic systems in general, Quan & Falkowskiare also concerned with the influence of ocean chemistry onthe evolution of marine organisms. They point out that theratios of dissolved fixed inorganic N to soluble inorganicphosphate (N:P) are relatively constant in the oceans but varyby up to two orders of magnitude in lakes. Quan & Falkowskipropose that these seemingly disparate observations can beunified by considering the role of the environment, in thiscase dissolved oxygen, on chemical and redox processesrelating to P solubility and N metabolism. This leads them tothe idea that the

δ

15

N signature of sedimentary organicmatter offers, under certain circumstances, a proxy for watercolumn oxidation state.

A striking illustration of the interactions between ‘green-house’ Earth and macroscopic aquatic plants is emergingfrom geochemical and palaeontological analyses of sedi-ments recovered from the Arctic Coring Expedition (ACEX)in 2004, as reported by Speelman

et

al

. These authorsestimate that a remarkable ‘bloom’ of the freshwater fern

Azolla

in the surface waters of the high arctic ocean duringthe Eocene (48.5 Ma) may have increased organic carbonburial by 1–3.5

×

10

18

g (1000–3500 Pg C, where 1 Pg = 10

18

g)over 1.2 million years. To place this number in context,it is estimated from satellite observations that Earth’sterrestrial and marine biospheres together annually fix

Email: d.j.beerling@Sheffield.ac.uk

98

D. J. BEERLING

© 2009 The AuthorJournal compilation © 2009 Blackwell Publishing Ltd

about 120 Pg C (Running

et

al

., 2004) of which onlyabout 2–3 Pg is sequestered and ultimately converted intofuture fossil fuel. According to Speelman

et

al.

, an Eocenefern feedback, taken at the scale of the entire Arctic Ocean,may have lowered atmospheric CO

2

concentrations by 200–450 p.p.m.

COEVOLUTION ON LAND

Raven & Giordano’s broad evolutionary view encompassesphotosynthetic organisms from cyanobacteria to vascular plantplants and considers evidence for their coevolution with theenvironment by focusing on biomineralization. In marineecosystems, it is apparent that silicification by successivelyevolving groups may be linked with declines in silicic acidconcentrations of the oceans; a change that perhaps reflectsbiological feedbacks on ocean chemistry. Indeed, diatomsnow dominate the ocean’s silica cycle and their evolutionaryhistory is thought to have influenced the radiation ofheterotrophs like sponges and radiolarians. Activities ofland plants are connected to oceanic events because, asRaven & Giordano point out, by weathering rocks theyprovide soluble substrates for biomineralization in inlandwater bodies and in the oceans. Silica production by grassesis especially important in this regard, exerting an impact onocean biogeochemistry.

Major trends in atmospheric CO

2

over the multimillion-yeartimescale of the Phanerozoic reflect the balance between CO

2

supply from volcanic degassing and its removal by the weatheringof silicate rocks, with the latter component subject to bioticintervention (Berner, 2006; Fletcher

et

al

., 2008). Pioneeringstudies identifying the role of the photosynthetic biosphere asan agent of this biotic intervention, by accelerating the weatheringof continental silicate rocks, have focused exclusively on landplants (reviewed in Berner

et

al

., 2003). However, the con-siderable body of emerging evidence drawn together by Taylor

et

al

. increasingly implicates the major groups of symbioticfungi that coevolved with plant roots as the primary agents ofbiotic weathering. The window on fungal weathering activitiesopened by Taylor

et

al.

together with emerging experimentalevidence (Leake

et

al

., 2008) sets the stage for an exciting secondphase in our detailed understanding of biotic weathering thatplaces a firm emphasis on fungal–mineral interactions drivenby photosynthetic energy.

Extending the linkage between photosynthesis and thegeosphere further, Franks & Beerling describe extensivequantitative analyses illustrating how variations in CO

2

influencedmaximum rates of stomatal-controlled water loss from leaves,both directly through the changes in the development ofstomata and indirectly through its effects on photosyntheticcapacity. They demonstrate that long-term atmospheric CO

2

variations likely drove the progressive increase in maximumleaf gas exchange capacity over 400 million years of land plantevolution. Taken in concert with the coevolution of water

conducting and rooting systems, the authors provocativelysuggest evolutionary changes in the maximum stomatalconductance and hydraulic capacity may be linked to the riseof land plant diversity seen in the rock record.

Boyce also turns to plant water relations and the localhydraulic environment within a canopy, in particular, todevelop ideas for distinguishing ‘sun’ and ‘shade’ leaves inthe fossil record. Traditionally, these two morphotypes areinterpreted as developmental responses to different irradianceregimes. Boyce’s studies with extant

Ginkgo

and

Quercus

trees highlight a possible role for hydraulic limitation onleaf expansion and vein density that may prove useful fordistinguishing ‘sun’ and ‘shade’ leaf morphotypes in thefossil record. Framed in the context of this study, geobiologyspans the integration of modern physiological ecology withpalaeobotany.

Moving from the scale of canopies to forests, DiMichele

et

al

. focus on identifying and interpreting feedbacks betweenancient forests and climate. In the late Palaeozoic (300–250 Ma),geological evidence indicates tropical terrestrial ecosystemsexperienced repeated warming and drying cycles before theEarth system ‘flipped’ to a more stable state. DiMichele

et

al

.document the evidence for this phenomenon and propose therole of vegetation in acting to stabilize the climatic transitionsprimarily through changes in land surface albedo and thehydrological cycle. The feedback of trace gases, such as methanefrom coal swamps (Beerling

et

al

., 2009), add a furtherfeedback of vegetation on climate at this time.

Finally, ascending the evolutionary tree to advanced landplants, Feild

et

al

. provide a thought-provoking overview ofangiosperm evolution that synthesizes information fromphylogenetics, palaeoecology and ecophysiology to suggesta new hypothesis for the emergence and success of thisgroup. They hypothesize that the early angiosperms werefundamentally intolerance of drought and that traits associatedwith this condition, including net-veined leaves, xylem vesselsand flowers, predisposed them to later selection for high pro-ductivity and diversity. Again, as with Glass

et

al

.’s hypothesisconcerning the metals involved in enzymatic N metabolism,aspects of this hypothesis can be tested with the applicationof modern plant physiological approaches on ancestralangiosperms.

CONCLUSION

On the evidence of this Special Issue, the field of geobiologyis increasingly being energized by the erosion of boundariesbetween scientific disciplines. Indeed, this is the only way forgeobiology to progress. These papers not only highlight thecoevolutionary nature of Earth’s biota and biogeochemicalprocesses but also our ability to decipher their signatures inextant organisms. Future research activities in interdisciplinaryterritories will be sure to stimulate further debate in this excitingnascent endeavour.

Coevolution of photosynthetic organisms and the environment

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© 2009 The AuthorJournal compilation © 2009 Blackwell Publishing Ltd

ACKNOWLEDGEMENTS

I thank all of the authors for their stimulating contributions tothis collection of articles, and the referees for taking the time toprovide critical and timely feedback to the authors. I gratefullyacknowledge funding of geobiological research in the Beerlinglab from the Natural Environment Research Council, UK, theLeverhulme Trust and the World Universities Network.

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